Satellite DNA-containing gigantic introns in a unique gene expression program during Drosophila spermatogenesis

PLoS Genet. 2019 May 9;15(5):e1008028. doi: 10.1371/journal.pgen.1008028. eCollection 2019 May.

Abstract

Intron gigantism, where genes contain megabase-sized introns, is observed across species, yet little is known about its purpose or regulation. Here we identify a unique gene expression program utilized for the proper expression of genes with intron gigantism. We find that two Drosophila genes with intron gigantism, kl-3 and kl-5, are transcribed in a spatiotemporal manner over the course of spermatocyte differentiation, which spans ~90 hours. The introns of these genes contain megabases of simple satellite DNA repeats that comprise over 99% of the gene loci, and these satellite-DNA containing introns are transcribed. We identify two RNA-binding proteins that specifically localize to kl-3 and kl-5 transcripts and are needed for the successful transcription or processing of these genes. We propose that genes with intron gigantism require a unique gene expression program, which may serve as a platform to regulate gene expression during cellular differentiation.

Publication types

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

MeSH terms

  • Animals
  • DNA, Satellite / genetics*
  • DNA, Satellite / metabolism
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism
  • Exons
  • Gene Expression Regulation, Developmental
  • Introns*
  • Male
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Signal Transduction
  • Spermatocytes / cytology
  • Spermatocytes / growth & development
  • Spermatocytes / metabolism*
  • Spermatogenesis / genetics*
  • Transcription, Genetic
  • Y Chromosome / chemistry

Substances

  • DNA, Satellite
  • Drosophila Proteins
  • RNA-Binding Proteins