Developmental dynamics of gene expression and alternative polyadenylation in the Caenorhabditis elegans germline

Genome Biol. 2018 Jan 24;19(1):8. doi: 10.1186/s13059-017-1369-x.

Abstract

Background: The 3' untranslated regions (UTRs) of mRNAs play a major role in post-transcriptional regulation of gene expression. Selection of transcript cleavage and polyadenylation sites is a dynamic process that produces multiple transcript isoforms for the same gene within and across different cell types. Using LITE-Seq, a new quantitative method to capture transcript 3' ends expressed in vivo, we have characterized sex- and cell type-specific transcriptome-wide changes in gene expression and 3'UTR diversity in Caenorhabditis elegans germline cells undergoing proliferation and differentiation.

Results: We show that nearly half of germline transcripts are alternatively polyadenylated, that differential regulation of endogenous 3'UTR variants is common, and that alternative isoforms direct distinct spatiotemporal protein expression patterns in vivo. Dynamic expression profiling also reveals temporal regulation of X-linked gene expression, selective stabilization of transcripts, and strong evidence for a novel developmental program that promotes nucleolar dissolution in oocytes. We show that the RNA-binding protein NCL-1/Brat is a posttranscriptional regulator of numerous ribosome-related transcripts that acts through specific U-rich binding motifs to down-regulate mRNAs encoding ribosomal protein subunits, rRNA processing factors, and tRNA synthetases.

Conclusions: These results highlight the pervasive nature and functional potential of patterned gene and isoform expression during early animal development.

Publication types

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

MeSH terms

  • 3' Untranslated Regions
  • Animals
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / genetics*
  • Caenorhabditis elegans Proteins / metabolism
  • Carrier Proteins / metabolism
  • Female
  • Gene Expression Regulation, Developmental*
  • Gonads / metabolism
  • Male
  • Nucleotide Motifs
  • Polyadenylation*
  • RNA Isoforms / metabolism
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins
  • Ribosomal Proteins / metabolism
  • Sequence Analysis, RNA / methods
  • Sex Characteristics

Substances

  • 3' Untranslated Regions
  • Caenorhabditis elegans Proteins
  • Carrier Proteins
  • RNA Isoforms
  • RNA, Messenger
  • RNA-Binding Proteins
  • Ribosomal Proteins
  • ncl-1 protein, C elegans