Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos

Science. 2011 Nov 25;334(6059):1141-4. doi: 10.1126/science.1210333. Epub 2011 Oct 13.

Abstract

The mitochondrial genome is believed to be maternally inherited in many eukaryotes. Sperm-derived paternal mitochondria enter the oocyte cytoplasm upon fertilization and then normally disappear during early embryogenesis. However, the mechanism responsible for this clearance has been unknown. Here, we show that autophagy, which delivers cytosolic components to lysosomes for degradation, is required for the elimination of paternal mitochondria in Caenorhabditis elegans. Immediately after fertilization, sperm-derived components trigger the localized induction of autophagy around sperm mitochondria. Autophagosomes engulf paternal mitochondria, resulting in their lysosomal degradation during early embryogenesis. In autophagy-defective zygotes, paternal mitochondria and their genome remain even in the first larval stage. Thus, fertilization-triggered autophagy is required for selective degradation of paternal mitochondria and thereby maternal inheritance of mitochondrial DNA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy*
  • Caenorhabditis elegans / embryology*
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / physiology
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • DNA, Helminth / analysis
  • DNA, Helminth / genetics
  • DNA, Mitochondrial / analysis
  • DNA, Mitochondrial / genetics
  • Embryo, Nonmammalian / physiology*
  • Embryonic Development
  • Fertilization*
  • Genome, Mitochondrial
  • Hermaphroditic Organisms
  • Lysosomes / metabolism
  • Male
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Mutation
  • Oocytes / physiology
  • Phagosomes / physiology*
  • Recombinant Fusion Proteins / metabolism
  • Spermatozoa / ultrastructure
  • Ubiquitination

Substances

  • Caenorhabditis elegans Proteins
  • DNA, Helminth
  • DNA, Mitochondrial
  • Recombinant Fusion Proteins