A sperm-oocyte protein partnership required for egg activation in Caenorhabditis elegans

Development. 2025 Jun 15;152(12):dev204674. doi: 10.1242/dev.204674. Epub 2025 Jun 25.

Abstract

Fertilization triggers the completion of female meiosis and launches the oocyte-to-embryo transition. Caenorhabditis elegans spe-11 is one of the few known paternal-effect embryonic lethal genes. We report that the sperm protein SPE-11 forms a complex with an oocyte protein, OOPS-1 (Oocyte Partner of SPE-11) at fertilization, and that the protein complex is required for the completion of meiosis, the block to polyspermy, and eggshell formation. Consistent with the molecular interaction of their encoded proteins, oops-1 and spe-11 exhibit indistinguishable null phenotypes in which fertilized oocytes arrest in meiosis I or meiosis II or fail to complete the actin-based process of meiotic cytokinesis. Biochemical analysis shows that the complex binds F-actin in the absence of other proteins and inhibits the nucleation of actin filaments at substoichiometric concentrations. Both OOPS-1 and SPE-11 are intrinsically disordered proteins that are highly phosphorylated, and biochemical and genetic experiments define interactions with the sperm-specific protein phosphatase 1 homologs GSP-3/4. Genetic results suggest that the cortical EGG complex recruits the OOPS-1-SPE-11 complex at fertilization, which promotes meiotic cytokinesis and in turn activates synthesis of the eggshell.

Keywords: Actin regulation; Egg activation; Fertilization; Meiotic cytokinesis; Oocyte meiosis.

MeSH terms

  • Actins / metabolism
  • Animals
  • Caenorhabditis elegans Proteins* / genetics
  • Caenorhabditis elegans Proteins* / metabolism
  • Caenorhabditis elegans* / embryology
  • Caenorhabditis elegans* / genetics
  • Caenorhabditis elegans* / metabolism
  • Caenorhabditis elegans* / physiology
  • Cytokinesis
  • Egg Proteins* / genetics
  • Egg Proteins* / metabolism
  • Female
  • Fertilization / physiology
  • Male
  • Meiosis / physiology
  • Oocytes* / cytology
  • Oocytes* / metabolism
  • Phosphorylation
  • Sperm-Ovum Interactions* / physiology
  • Spermatozoa* / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • Actins
  • Egg Proteins