Abstract
Quiescent cells (Q) are seemingly inactive, developmentally arrested cells, whose universal characteristic is the ability to promptly reenter 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, 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.