Distinct cis-acting elements mediate targeting and clustering of Drosophila polar granule mRNAs

Development. 2018 Nov 22;145(22):dev164657. doi: 10.1242/dev.164657.

Abstract

Specification and development of Drosophila germ cells depend on molecular determinants within the germ plasm, a specialized cytoplasmic domain at the posterior of the embryo. Localization of numerous mRNAs to the germ plasm occurs by their incorporation, as single-transcript ribonucleoprotein (RNP) particles, into complex RNP granules called polar granules. Incorporation of mRNAs into polar granules is followed by recruitment of additional like transcripts to form discrete homotypic clusters. The cis-acting localization signals that target mRNAs to polar granules and promote homotypic clustering remain largely uncharacterized. Here, we show that the polar granule component (pgc) and germ cell-less (gcl) 3' untranslated regions contain complex localization signals comprising multiple, independently weak and partially functionally redundant localization elements (LEs). We demonstrate that targeting of pgc to polar granules and self-assembly into homotypic clusters are functionally separable processes mediated by distinct classes of LEs. We identify a sequence motif shared by other polar granule mRNAs that contributes to homotypic clustering. Our results suggest that mRNA localization signal complexity may be a feature required by the targeting and self-recruitment mechanism that drives germ plasm mRNA localization.

Keywords: Drosophila; Germ plasm; Polar granule; gcl; mRNA localization; pgc.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • 3' Untranslated Regions / genetics
  • Animals
  • Base Pairing
  • Cell Polarity / genetics*
  • Conserved Sequence / genetics
  • Cytoplasmic Granules / metabolism*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics*
  • Intercellular Signaling Peptides and Proteins
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Nucleotide Motifs / genetics
  • Positive Transcriptional Elongation Factor B / genetics
  • Positive Transcriptional Elongation Factor B / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Regulatory Sequences, Nucleic Acid / genetics*

Substances

  • 3' Untranslated Regions
  • Drosophila Proteins
  • Intercellular Signaling Peptides and Proteins
  • Nuclear Proteins
  • RNA, Messenger
  • gcl protein, Drosophila
  • pgc protein, Drosophila
  • Positive Transcriptional Elongation Factor B