Intergenic accumulation of RNA polymerase II maintains the potential for swift transcriptional restart upon release from quiescence
- Manuela Baquero Pérez1,
- Gertjan Laenen1,3,
- Isabelle Loïodice1,3,
- Mickaël Garnier1,
- Ugo Szachnowski2,
- Antonin Morillon2,
- Myriam Ruault1 and
- Angela Taddei1
- 1UMR 3664 Nuclear Dynamics, CNRS, Institut Curie, Université PSL, Sorbonne University, 75248 Paris, France;
- 2UMR 3244 DIG-Cancer, CNRS, Institut Curie, Université PSL, Sorbonne University, 75248 Paris, France
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↵3 These authors contributed equally to this work.
Abstract
Quiescent (Q) cells are seemingly inactive, developmentally arrested cells, whose universal characteristic is the ability to promptly re-enter the cell cycle upon sensing of external cues. Q cells are responsive to the environment and flexible enough to adapt to available resources. In budding yeast, quiescent nuclear features are drastically distinct from those observed in nutrient replete conditions: The nuclear volume is reduced; the telomeres relocate from the nuclear periphery to the center of the nucleus into a hypercluster; chromatin is found in a compacted, hypoacetylated state; and transcription is globally shutdown. Yet, Q cells can restart transcription within minutes of refeeding. Here, we follow the global decrease of transcription in sorted, developing Q populations and its reactivation upon release. We find that transcription and telomere clustering dynamics in and out of quiescence are independent events. We report a genome-wide redistribution of the transcription machinery as cells progress into quiescence. Although most genes are shut down, 3% of coding genes remain active. Furthermore, RNA polymerase II (RNAPII) accumulates at one-third of gene promoters. The corresponding genes are highly enriched among those showing a high level of transcription and high frequency of expression in individual cells, shortly after cells are refed, as monitored by single-cell RNA-seq. Our results point toward a role for quiescent-specific RNAPII distribution to ensure a rapid and robust transcriptional response upon return to growth.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.279874.124.
- Received August 2, 2024.
- Accepted August 4, 2025.
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