Abstract

SummaryDuring Caenorhabditis elegans oocyte meiosis, a multi-protein ring complex (RC) localized between homologous chromosomes, promotes chromosome congression through the action of the chromokinesin KLP-19. While some RC components are known, the mechanism of RC assembly has remained obscure. We show that SUMO E3 ligase GEI-17/PIAS is required for KLP-19 recruitment to the RC, and proteomic analysis identified KLP-19 as a SUMO substrate in vivo. In vitro analysis revealed that KLP-19 is efficiently sumoylated in a GEI-17-dependent manner, while GEI-17 undergoes extensive auto-sumoylation. GEI-17 and another RC component, the kinase BUB-1, contain functional SUMO interaction motifs (SIMs), allowing them to recruit SUMO modified proteins, including KLP-19, into the RC. Thus, dynamic SUMO modification and the presence of SIMs in RC components generate a SUMO-SIM network that facilitates assembly of the RC. Our results highlight the importance of SUMO-SIM networks in regulating the assembly of dynamic protein complexes.

Highlights

  • Meiosis is a specialized division in which a single round of DNA replication is followed by two consecutive segregation steps

  • small ubiquitin-related modifier (SUMO) in the C. elegans Germline While sumoylation plays a role in meiotic chromosome pairing during prophase in yeast, this is not conserved in nematodes, where synapsis occurs normally in the absence of SUMO (Bhalla et al, 2008)

  • While SUMO knockout worms have severe germline defects (Broday et al, 2004), we found that in SUMO E3 ligase gei-17 À/À worms, some oocytes mature in spite of the defective germline and accumulate the chromosomal passenger complex (CPC) protein ICP-1 in the midbivalent and the cohesin REC-8 between homologous chromosomes and sister chromatids (Figure S1A)

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Summary

Introduction

Meiosis is a specialized division in which a single round of DNA replication is followed by two consecutive segregation steps. As meiotic spindles vary across the animal kingdom, identification of common and unique mechanisms of spindle assembly and chromosome orientation, congression, and segregation will contribute to the fundamental understanding of these processes (Dumont and Desai, 2012; Severson et al, 2016). In C. elegans oocytes, chromosome movement along lateral microtubule bundles is facilitated by plus-end directed forces exerted by the kinesin KLP-19 (Powers et al., 2004; Wignall and Villeneuve, 2009), which requires the kinase BUB-1 for localization to the ring complex (RC). BUB-1, in turn, requires the chromosomal passenger complex (CPC) components AIR-2/Aurora B and ICP-1/INCENP for RC localization (Dumont et al, 2010; Wignall and Villeneuve, 2009).

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