A Novel Role for α-Importins and Akirin in Establishment of Meiotic Sister Chromatid Cohesion in Caenorhabditis elegans

Richard Bowman; Nathan Balukof; Talitha Ford; Sarit Smolikove

doi:10.1534/genetics.118.301458

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A Novel Role for α-Importins and Akirin in Establishment of Meiotic Sister Chromatid Cohesion in Caenorhabditis elegans

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A Novel Role for α-Importins and Akirin in Establishment of Meiotic Sister Chromatid Cohesion in Caenorhabditis elegans

Richard Bowman, Nathan Balukof, Talitha Ford and Sarit Smolikove

Genetics (Austin), Vol.211(2), pp.617-635

02/2019

DOI: 10.1534/genetics.118.301458

PMCID: PMC6366927

PMID: 30563860

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https://doi.org/10.25386/genetics.7471409View

Published (Version of record) Open Access

Abstract

During meiotic prophase I, sister chromatid cohesion is established in a way that supports the assembly of the synaptonemal complex (SC). The SC connects homologous chromosomes, directing meiotic recombination to create crossovers. In this paper, we identify two proteins that cooperate to import and load meiotic cohesins, thus indirectly promoting SC assembly. AKIR-1 is a protein with a previously identified meiotic role in SC disassembly. akir-1 mutants have no obvious defects in sister chromatid cohesion. We identified ima-2, a gene encoding for an α-importin nuclear transport protein, as a gene interacting with akir-1. Analysis of akir-1;ima-2 double mutants reveals a decrease in the number of germline nuclei and the formation of polycomplexes (PCs) (an SC protein aggregate). These PCs contain proteins that are part of the two main substructures of the SC: the central region and the lateral element. Unlike typical PCs, they also contain sister chromatid cohesion proteins. In akir-1;ima-2 double mutants, PCs are located in both the nucleus and the cytoplasm. This suggests that the defects observed in the double mutants are both in nuclear import and in the assembly of sister chromatid cohesion. PC formation is also associated with recombination defects leading to reduced numbers of crossovers. Similarly to cohesion mutants, the pairing center protein HIM-8 is mislocalized in akir-1;ima-2 double mutants, forming multiple foci. We propose that AKIR-1 and IMA-2 operate in parallel pathways to import and load chromosomally associated cohesin complex proteins in meiotic nuclei, a novel finding for both of these conserved proteins.

Mutation

Caenorhabditis elegans - genetics

Chromatids - genetics

Cell Cycle Proteins - metabolism

Caenorhabditis elegans Proteins - metabolism

Meiosis

Synaptonemal Complex - genetics

Synaptonemal Complex - metabolism

Chromatids - metabolism

Animals

Karyopherins - metabolism

Cell Cycle Proteins - genetics

Karyopherins - genetics

Protein Binding

Sister Chromatid Exchange

Germ Cells - cytology

Germ Cells - metabolism

Caenorhabditis elegans Proteins - genetics

akir-1

ima-2

akirin

coh-3/4

Details

Title: Subtitle: A Novel Role for α-Importins and Akirin in Establishment of Meiotic Sister Chromatid Cohesion in Caenorhabditis elegans
Creators: Richard Bowman - Department of Biology, University of Iowa, Iowa City, Iowa 52240
Nathan Balukof - Department of Biology, University of Iowa, Iowa City, Iowa 52240
Talitha Ford - Department of Biology, University of Iowa, Iowa City, Iowa 52240
Sarit Smolikove - Department of Biology, University of Iowa, Iowa City, Iowa 52240 sarit-smolikove@uiowa.edu
Resource Type: Journal article
Publication Details: Genetics (Austin), Vol.211(2), pp.617-635
DOI: 10.1534/genetics.118.301458
PMID: 30563860
PMCID: PMC6366927
NLM abbreviation: Genetics
ISSN: 0016-6731
eISSN: 1943-2631
Publisher: United States
Grant note: P40 OD010440 / NIH HHS
Language: English
Date published: 02/2019
Academic Unit: Biology
Record Identifier: 9983992055202771

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