Distinct histone methylation and transcription profiles are established during the development of cellular quiescence in yeast

Abstract

BackgroundQuiescent cells have a low level of gene activity compared to growing cells. Using a yeast model for cellular quiescence, we defined the genome-wide profiles of three species of histone methylation associated with active transcription between growing and quiescent cells, and correlated these profiles with the presence of RNA polymerase II and transcripts.ResultsQuiescent cells retained histone methylations normally associated with transcriptionally active chromatin and had many transcripts in common with growing cells. Quiescent cells also contained significant levels of RNA polymerase II, but only low levels of the canonical initiating and elongating forms of the polymerase. The RNA polymerase II associated with genes in quiescent cells displayed a distinct occupancy profile compared to its pattern of occupancy across genes in actively growing cells. Although transcription is generally repressed in quiescent cells, analysis of individual genes identified a period of active transcription during the development of quiescence.ConclusionsThe data suggest that the transcript profile and histone methylation marks in quiescent cells were established both in growing cells and during the development of quiescence and then retained in these cells. Together, this might ensure that quiescent cells can rapidly adapt to a changing environment to resume growth.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3509-9) contains supplementary material, which is available to authorized users.

Metabolic switches from quiescence to growth in synchronized Saccharomyces cerevisiae

“…Transcriptome analysis of quiescence exit in shake flask cultures showed an immediate upregulation of at least 2500 genes within 360 s (Radonjic et al 2005). Distinct histone methylation and transcription profiles were observed for quiescence in yeast, which can rapidly be reversed and resume growth (Young et al 2017). Laporte et al found that the metabolic status and flux rather than cell cycle regulators are the principal triggers for the quiescence exit.…”

Ssd1 and the cell wall integrity pathway promote entry, maintenance, and recovery from quiescence in budding yeast

“…In Saccharomyces cerevisiae , quiescence is typically induced by nutrient limitation, but it is not a starvation state. Faced with a waning nutrient supply, these cells down-regulate highly conserved signaling pathways that promote proliferation and redirect their gene expression and metabolism to stockpile nutrients and induce processes that promote long-term survival (Lillie and Pringle, 1980; Sillje et al ., 1999; Francois and Parrou, 2001; De Virgilio, 2012; McKnight et al ., 2015; Young et al ., 2017).…”

Division of labour in the yeast: Saccharomyces cerevisiae

“…The other cells in the population are non‐quiescent (NQ) and may continue proliferating. The organization of a Q cell's internal structures and genome is very different from that of a NQ cell – there is an increase in the storage carbohydrates and stress protectants glycogen and trehalose, an increased width of the cell wall (Aragon et al ., ), sequestration of proteins (Suresh et al ., ), telomere clustering (Guidi et al ., ; Laporte et al ., ; Rutledge et al ., ) and transcriptional shut down (McKnight et al ., ; Young et al ., ). The most significant evolutionary property of yeast quiescent cells is their ability to maintain viability over long periods of time during the growth‐arrested phase and to resume mitotic growth once growth‐promoting conditions are restored (Gray et al ., ).…”