Compartmentalized oskar degradation in the germ plasm safeguards germline development

Elife. 2020 Jan 7:9:e49988. doi: 10.7554/eLife.49988.

Abstract

Partitioning of mRNAs into ribonucleoprotein (RNP) granules supports diverse regulatory programs within the crowded cytoplasm. At least two types of RNP granules populate the germ plasm, a cytoplasmic domain at the posterior of the Drosophila oocyte and embryo. Germ granules deliver mRNAs required for germline development to pole cells, the germ cell progenitors. A second type of RNP granule, here named founder granules, contains oskar mRNA, which encodes the germ plasm organizer. Whereas oskar mRNA is essential for germ plasm assembly during oogenesis, we show that it is toxic to pole cells. Founder granules mediate compartmentalized degradation of oskar during embryogenesis to minimize its inheritance by pole cells. Degradation of oskar in founder granules is temporally and mechanistically distinct from degradation of oskar and other mRNAs during the maternal-to-zygotic transition. Our results show how compartmentalization in RNP granules differentially controls fates of mRNAs localized within the same cytoplasmic domain.

Keywords: D. melanogaster; RNA granule; developmental biology; founder granule; germ plasm; mRNA degradation; oskar; ribonucleoprotein.

MeSH terms

  • Animals
  • Cell Compartmentation*
  • Cell Movement
  • Cytoplasmic Granules / metabolism
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / cytology*
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / metabolism
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / metabolism
  • Female
  • Germ Cells / cytology*
  • Germ Cells / metabolism*
  • Peptide Initiation Factors / metabolism
  • Proteolysis*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism

Substances

  • Drosophila Proteins
  • Peptide Initiation Factors
  • RNA, Messenger
  • aub protein, Drosophila
  • osk protein, Drosophila