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

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 transcri...

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Main Authors: Yicheng Luo, Elena Fefelova, Maria Ninova, Yung-Chia Ariel Chen, Alexei A Aravin
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/52416
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spelling doaj-90a5ffe5b8d64cc89627554c1e1d90e82021-05-05T21:41:33ZengeLife Sciences Publications LtdeLife2050-084X2020-11-01910.7554/eLife.52416Repression of interrupted and intact rDNA by the SUMO pathway in Drosophila melanogasterYicheng Luo0https://orcid.org/0000-0003-3704-2389Elena Fefelova1https://orcid.org/0000-0002-9185-1243Maria Ninova2Yung-Chia Ariel Chen3Alexei A Aravin4https://orcid.org/0000-0002-6956-8257Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United StatesDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States; Institute of Molecular Genetics, Russian Academy of Sciences, Moscow, Russian FederationDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, United StatesDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, United StatesDivision of Biology and Biological Engineering, California Institute of Technology, Pasadena, United StatesRibosomal 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.https://elifesciences.org/articles/52416rDNASUMOepigenetic regulationtransposondifferential expression
collection DOAJ
language English
format Article
sources DOAJ
author Yicheng Luo
Elena Fefelova
Maria Ninova
Yung-Chia Ariel Chen
Alexei A Aravin
spellingShingle Yicheng Luo
Elena Fefelova
Maria Ninova
Yung-Chia Ariel Chen
Alexei A Aravin
Repression of interrupted and intact rDNA by the SUMO pathway in Drosophila melanogaster
eLife
rDNA
SUMO
epigenetic regulation
transposon
differential expression
author_facet Yicheng Luo
Elena Fefelova
Maria Ninova
Yung-Chia Ariel Chen
Alexei A Aravin
author_sort Yicheng Luo
title Repression of interrupted and intact rDNA by the SUMO pathway in Drosophila melanogaster
title_short Repression of interrupted and intact rDNA by the SUMO pathway in Drosophila melanogaster
title_full Repression of interrupted and intact rDNA by the SUMO pathway in Drosophila melanogaster
title_fullStr Repression of interrupted and intact rDNA by the SUMO pathway in Drosophila melanogaster
title_full_unstemmed Repression of interrupted and intact rDNA by the SUMO pathway in Drosophila melanogaster
title_sort repression of interrupted and intact rdna by the sumo pathway in drosophila melanogaster
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-11-01
description 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.
topic rDNA
SUMO
epigenetic regulation
transposon
differential expression
url https://elifesciences.org/articles/52416
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AT elenafefelova repressionofinterruptedandintactrdnabythesumopathwayindrosophilamelanogaster
AT marianinova repressionofinterruptedandintactrdnabythesumopathwayindrosophilamelanogaster
AT yungchiaarielchen repressionofinterruptedandintactrdnabythesumopathwayindrosophilamelanogaster
AT alexeiaaravin repressionofinterruptedandintactrdnabythesumopathwayindrosophilamelanogaster
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