A bifunctional snoRNA with separable activities in guiding rRNA 2’-O-methylation and scaffolding gametogenesis effectors

Estelle Leroy, Drice Challal, Stéphane Pelletier, Coralie Goncalves, Alexandra Menant, Virginie Marchand, Yan Jaszczyszyn, Erwin Dijk, Delphine Naquin, Jessica Andreani, Yuri Motorin, Benoit Palancade and Mathieu Rougemaille ()
Additional contact information
Estelle Leroy: Institute for Integrative Biology of the Cell (I2BC)
Drice Challal: Institute for Integrative Biology of the Cell (I2BC)
Stéphane Pelletier: Institute for Integrative Biology of the Cell (I2BC)
Coralie Goncalves: Institut Jacques Monod
Alexandra Menant: Institute for Integrative Biology of the Cell (I2BC)
Virginie Marchand: Epitranscriptomics and RNA sequencing (EpiRNA-Seq) Core Facility (SMP IBSLor) and UMR7365 IMoPA CNRS
Yan Jaszczyszyn: Institute for Integrative Biology of the Cell (I2BC)
Erwin Dijk: Institute for Integrative Biology of the Cell (I2BC)
Delphine Naquin: Institute for Integrative Biology of the Cell (I2BC)
Jessica Andreani: Institute for Integrative Biology of the Cell (I2BC)
Yuri Motorin: Epitranscriptomics and RNA sequencing (EpiRNA-Seq) Core Facility (SMP IBSLor) and UMR7365 IMoPA CNRS
Benoit Palancade: Institut Jacques Monod
Mathieu Rougemaille: Institute for Integrative Biology of the Cell (I2BC)

Nature Communications, 2025, vol. 16, issue 1, 1-18

Abstract: Abstract Small nucleolar RNAs are non-coding transcripts that guide chemical modifications of RNA substrates and modulate gene expression at the epigenetic and post-transcriptional levels. However, the extent of their regulatory potential and the underlying molecular mechanisms remain poorly understood. Here, we identify a conserved, previously unannotated intronic C/D-box snoRNA, termed snR107, hosted in the fission yeast long non-coding RNA mamRNA and carrying two independent cellular functions. On the one hand, snR107 guides site-specific 25S rRNA 2’-O-methylation and promotes pre-rRNA processing and 60S subunit biogenesis. On the other hand, snR107 associates with the gametogenic RNA-binding proteins Mmi1 and Mei2, mediating their reciprocal inhibition and restricting meiotic gene expression during sexual differentiation. Both functions require distinct cis-motifs within snR107, including a conserved 2’-O-methylation guiding sequence. Together, our results position snR107 as a dual regulator of rRNA modification and gametogenesis effectors, expanding our vision on the non-canonical functions exerted by snoRNAs in cell fate decisions.

Date: 2025
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DOI: 10.1038/s41467-025-58664-y

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