Extensive nuclear gyration and pervasive non-genic transcription during primordial germ cell development in zebrafish

Development. 2021 Jan 20;148(2):dev193060. doi: 10.1242/dev.193060.

Abstract

Primordial germ cells (PGCs) are the precursors of germ cells, which migrate to the genital ridge during early development. Relatively little is known about PGCs after their migration. We studied this post-migratory stage using microscopy and sequencing techniques, and found that many PGC-specific genes, including genes known to induce PGC fate in the mouse, are only activated several days after migration. At this same time point, PGC nuclei become extremely gyrated, displaying general broad opening of chromatin and high levels of intergenic transcription. This is accompanied by changes in nuage morphology, expression of large loci (PGC-expressed non-coding RNA loci, PERLs) that are enriched for retro-transposons and piRNAs, and a rise in piRNA biogenesis signatures. Interestingly, no nuclear Piwi protein could be detected at any time point, indicating that the zebrafish piRNA pathway is fully cytoplasmic. Our data show that the post-migratory stage of zebrafish PGCs holds many cues to both germ cell fate establishment and piRNA pathway activation.

Keywords: Gyration; Intergenic transcription; Nuage; Nuclear morphology; Primordial germ cell; Zebrafish; Zygotic activation; piRNA.

MeSH terms

  • Animals
  • Cell Nucleus / genetics*
  • Cell Nucleus / ultrastructure
  • DNA Transposable Elements / genetics
  • DNA, Intergenic / genetics
  • DNA-Directed RNA Polymerases / metabolism
  • Fertilization
  • Gene Expression Regulation, Developmental
  • Genetic Loci
  • Germ Cells / metabolism*
  • Germ Cells / ultrastructure
  • Mutation / genetics
  • RNA, Small Interfering / metabolism
  • RNA, Untranslated / genetics
  • RNA, Untranslated / metabolism
  • Transcription, Genetic*
  • Up-Regulation / genetics
  • Zebrafish / genetics*
  • Zebrafish Proteins / genetics
  • Zebrafish Proteins / metabolism
  • Zygote / metabolism

Substances

  • DNA Transposable Elements
  • DNA, Intergenic
  • RNA, Small Interfering
  • RNA, Untranslated
  • Zebrafish Proteins
  • DNA-Directed RNA Polymerases