Cortical microtubule pulling forces contribute to the union of the parental genomes in the Caenorhabditis elegans zygote

Elife. 2022 Mar 8:11:e75382. doi: 10.7554/eLife.75382.

Abstract

Previously, we reported that the Polo-like kinase PLK-1 phosphorylates the single Caenorhabditis elegans lamin (LMN-1) to trigger lamina depolymerization during mitosis. We showed that this event is required to form a pronuclear envelope scission event that removes membranes on the juxtaposed oocyte and sperm pronuclear envelopes in the zygote, allowing the parental chromosomes to merge in a single nucleus after segregation (Velez-Aguilera et al., 2020). Here, we show that cortical microtubule pulling forces contribute to pronuclear envelopes scission by promoting mitotic spindle elongation, and conversely, nuclear envelopes remodeling facilitates spindle elongation. We also demonstrate that weakening the pronuclear envelopes via PLK-1-mediated lamina depolymerization, is a prerequisite for the astral microtubule pulling forces to trigger pronuclear membranes scission. Finally, we provide evidence that PLK-1 mainly acts via lamina depolymerization in this process. These observations thus indicate that temporal coordination between lamina depolymerization and mitotic spindle elongation facilitates pronuclear envelopes scission and parental genomes unification.

Keywords: C. elegans; cell biology; microtubules; nuclear envelope; polo-like kinase; union parental chromosomes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans Proteins* / genetics
  • Caenorhabditis elegans* / genetics
  • Embryo, Nonmammalian
  • Laminin / genetics
  • Microtubules
  • Mitosis
  • Protein Serine-Threonine Kinases / genetics
  • Spindle Apparatus
  • Zygote

Substances

  • Caenorhabditis elegans Proteins
  • LMN-1 protein, C elegans
  • Laminin
  • Protein Serine-Threonine Kinases
  • plk-1 protein, C elegans

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.