Repression of interrupted and intact rDNA by the SUMO pathway in Drosophila melanogaster

Elife. 2020 Nov 9:9:e52416. doi: 10.7554/eLife.52416.


Ribosomal RNAs (rRNAs) are essential components of the ribosome and are among the most abundant macromolecules in the cell. To ensure high rRNA level, eukaryotic genomes contain dozens to hundreds of rDNA genes, however, only a fraction of the rRNA genes seems to be active, while others are transcriptionally silent. We found that individual rDNA genes have high level of cell-to-cell heterogeneity in their expression in Drosophila melanogaster. Insertion of heterologous sequences into rDNA leads to repression associated with reduced expression in individual cells and decreased number of cells expressing rDNA with insertions. We found that SUMO (Small Ubiquitin-like Modifier) and SUMO ligase Ubc9 are required for efficient repression of interrupted rDNA units and variable expression of intact rDNA. Disruption of the SUMO pathway abolishes discrimination of interrupted and intact rDNAs and removes cell-to-cell heterogeneity leading to uniformly high expression of individual rDNA in single cells. Our results suggest that the SUMO pathway is responsible for both repression of interrupted units and control of intact rDNA expression.

Keywords: D. melanogaster; SUMO; chromosomes; differential expression; epigenetic regulation; gene expression; genetics; genomics; rDNA; transposon.

Publication types

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

MeSH terms

  • Animals
  • DNA Transposable Elements
  • DNA, Ribosomal / metabolism*
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / metabolism
  • Gene Expression Regulation
  • Genes, rRNA*
  • Heterochromatin / metabolism
  • Metabolic Networks and Pathways
  • Models, Genetic
  • Nuclear Proteins / metabolism
  • Repressor Proteins / metabolism*
  • Small Ubiquitin-Related Modifier Proteins
  • Transgenes
  • Ubiquitin-Conjugating Enzymes / metabolism


  • DNA Transposable Elements
  • DNA, Ribosomal
  • Drosophila Proteins
  • Heterochromatin
  • Nuclear Proteins
  • Repressor Proteins
  • Small Ubiquitin-Related Modifier Proteins
  • smt3 protein, Drosophila
  • Ubiquitin-Conjugating Enzymes
  • ubiquitin-conjugating enzyme UBC9

Associated data

  • GEO/GSE141068
  • GEO/GSE115277
  • GEO/GSE55303