A SUMO E3 ligase promotes long non-coding RNA transcription to regulate small RNA-directed DNA elimination

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Abstract

Small RNAs target their complementary chromatin regions for gene silencing through nascent long non-coding RNAs (lncRNAs). In the ciliated protozoan Tetrahymena, the interaction between Piwi-associated small RNAs (scnRNAs) and the nascent lncRNA transcripts from the somatic genome has been proposed to induce target-directed small RNA degradation (TDSD), and scnRNAs not targeted for TDSD later target the germline-limited sequences for programmed DNA elimination. In this study, we show that the SUMO E3 ligase Ema2 is required for the accumulation of lncRNAs from the somatic genome and thus for TDSD and completing DNA elimination to make viable sexual progeny. Ema2 interacts with the SUMO E2 conjugating enzyme Ubc9 and enhances SUMOylation of the transcription regulator Spt6. We further show that Ema2 promotes the association of Spt6 and RNA polymerase II with chromatin. These results suggest that Ema2-directed SUMOylation actively promotes lncRNA transcription, which is a prerequisite for communication between the genome and small RNAs.

Data availability

Data DepositionThe small RNA sequencing data have been deposited in the Gene Expression Omnibus (GEO) database, https://www.ncbi.nlm.nih.gov/geo (accession no. GSE243435). The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the MassIVE partner repository (https://massive.ucsd.edu/) with the database identifier MSV000092977.

The following data sets were generated

(2023) A SUMO E3 ligase promotes long non-coding RNA transcription to regulate small RNA-directed DNA elimination
NCBI Gene Expression Omnibus, GSE243435.

http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE243435

Article and author information

Author details

Salman Shehzada

Institute of Human Genetics, University of Montpellier, CNRS, Montpellier, France

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4218-7622
Tomoko Noto

Institute of Human Genetics, University of Montpellier, CNRS, Montpellier, France

Competing interests
The authors declare that no competing interests exist.
Julie Saksouk

Institute of Human Genetics (IGH), University of Montpellier, CNRS, Montpellier, France

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-1885-1762
Kazufumi Mochizuki

Institute of Human Genetics, University of Montpellier, CNRS, Montpellier, France

For correspondence
kazufumi.mochizuki@cnrs.fr

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-7987-9852

Funding

Agence Nationale de la Recherche (ANR-10-INBS-04)

Kazufumi Mochizuki

Agence Nationale de la Recherche (ANR-10-LABX-12-01)

Kazufumi Mochizuki

Agence Nationale de la Recherche (ANR-16-ACHN-0017)

Kazufumi Mochizuki

Fondation pour la Recherche Médicale

Salman Shehzada

Foundation Recherche Médicale (EQU202203014651)

Kazufumi Mochizuki

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.