Fndc-1 contributes to paternal mitochondria elimination in C. elegans

Dev Biol. 2019 Oct 1;454(1):15-20. doi: 10.1016/j.ydbio.2019.06.016. Epub 2019 Jun 21.

Abstract

Paternal mitochondria are eliminated following fertilization by selective autophagy, but the mechanisms that restrict this process to sperm-derived organelles are not well understood. FUNDC1 (FUN14 domain containing 1) is a mammalian mitophagy receptor expressed on the mitochondrial outer membrane that contributes to mitochondrial quality control following hypoxic stress. Like FUNDC1, the C. elegans ortholog FNDC-1 is widely expressed in somatic tissues and mediates hypoxic mitophagy. Here, we report that FNDC-1 is strongly expressed in sperm but not oocytes and contributes to paternal mitochondria elimination. Paternal mitochondrial DNA is normally undetectable in wildtype larva, but can be detected in the cross-progeny of fndc-1 mutant males. Moreover, loss of fndc-1 retards the rate of paternal mitochondria degradation, but not that of membranous organelles, a nematode specific membrane compartment whose fusion is required for sperm motility. This is the first example of a ubiquitin-independent mitophagy receptor playing a role in the selective degradation of sperm mitochondria.

Keywords: Autophagy; C. elegans; Maternal inheritance; Mitochondria; Mitophagy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy / genetics
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / metabolism*
  • DNA, Mitochondrial / genetics
  • Embryo, Nonmammalian / metabolism
  • Fertilization
  • Humans
  • Lysosomes / metabolism
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Mitochondrial Membranes / metabolism
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Mitophagy / physiology
  • Oocytes / metabolism
  • Organelles / metabolism
  • Sperm Motility
  • Spermatozoa / metabolism
  • Ubiquitin / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • DNA, Mitochondrial
  • FUNDC1 protein, human
  • Membrane Proteins
  • Mitochondrial Proteins
  • Ubiquitin