Germ Granules Prevent Accumulation of Somatic Transcripts in the Adult Caenorhabditis elegans Germline

Genetics. 2017 May;206(1):163-178. doi: 10.1534/genetics.116.198549. Epub 2017 Mar 3.

Abstract

The germ cells of multicellular organisms protect their developmental potential through specialized mechanisms. A shared feature of germ cells from worms to humans is the presence of nonmembrane-bound, ribonucleoprotein organelles called germ granules. Depletion of germ granules in Caenorhabditis elegans (i.e., P granules) leads to sterility and, in some germlines, expression of the neuronal transgene unc-119::gfp and the muscle myosin MYO-3 Thus, P granules are hypothesized to maintain germ cell totipotency by preventing somatic development, although the mechanism by which P granules carry out this function is unknown. In this study, we performed transcriptome and single molecule RNA-FISH analyses of dissected P granule-depleted gonads at different developmental stages. Our results demonstrate that P granules are necessary for adult germ cells to downregulate spermatogenesis RNAs and to prevent the accumulation of numerous soma-specific RNAs. P granule-depleted gonads that express the unc-119::gfp transgene also express many other genes involved in neuronal development and concomitantly lose expression of germ cell fate markers. Finally, we show that removal of either of two critical P-granule components, PGL-1 or GLH-1, is sufficient to cause germ cells to express UNC-119::GFP and MYO-3 and to display RNA accumulation defects similar to those observed after depletion of P granules. Our data identify P granules as critical modulators of the germline transcriptome and guardians of germ cell fate.

Keywords: Caenorhabditis elegans; GLH-1; P granules; PGL-1; germ-soma antagonism; germline.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans Proteins / biosynthesis
  • Caenorhabditis elegans Proteins / genetics*
  • Cytoplasmic Granules / genetics
  • Cytoplasmic Granules / metabolism
  • DEAD-box RNA Helicases / genetics*
  • Gene Expression Regulation
  • Germ Cells / metabolism
  • Infertility / genetics*
  • Infertility / pathology
  • Nerve Tissue Proteins / biosynthesis
  • Nerve Tissue Proteins / genetics*
  • RNA / genetics
  • RNA / metabolism
  • RNA-Binding Proteins / genetics*
  • Ribonucleoproteins / genetics
  • Spermatogenesis / genetics
  • Transcriptome / genetics

Substances

  • Caenorhabditis elegans Proteins
  • Nerve Tissue Proteins
  • PGL-1 protein, C elegans
  • RNA-Binding Proteins
  • Ribonucleoproteins
  • UNC-119 protein, C elegans
  • RNA
  • GLH-1 protein, C elegans
  • DEAD-box RNA Helicases