A paternal protein facilitates sperm RNA delivery to regulate zygotic development

Sci China Life Sci. 2023 Oct;66(10):2342-2353. doi: 10.1007/s11427-022-2332-5. Epub 2023 May 6.

Abstract

Sperm contributes essential paternal factors, including the paternal genome, centrosome, and oocyte-activation signals, to sexual reproduction. However, it remains unresolved how sperm contributes its RNA molecules to regulate early embryonic development. Here, we show that the Caenorhabditis elegans paternal protein SPE-11 assembles into granules during meiotic divisions of spermatogenesis and later matures into a perinuclear structure where sperm RNAs localize. We reconstitute an SPE-11 liquid-phase scaffold in vitro and find that SPE-11 condensates incorporate the nematode RNA, which, in turn, promotes SPE-11 phase separation. Loss of SPE-11 does not affect sperm motility or fertilization but causes pleiotropic development defects in early embryos, and spe-11 mutant males reduce mRNA levels of genes crucial for an oocyte-to-embryo transition or embryonic development. These results reveal that SPE-11 undergoes phase separation and associates with sperm RNAs that are delivered to oocytes during fertilization, providing insights into how a paternal protein regulates early embryonic development.

Keywords: SPE-11; early embryonic development; paternal factor; phase separation.

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Fertilization
  • Male
  • Oocytes
  • RNA* / genetics
  • RNA* / metabolism
  • Semen*
  • Sperm Motility
  • Spermatogenesis / genetics
  • Spermatozoa / metabolism

Substances

  • RNA