Long Noncoding RNAs Promote Transcriptional Poising of Inducible Genes

Sara C Cloutier,Siwen Wang,Christopher J Petell,Wai Kit Ma,Elizabeth J Tran,Fred Winston

doi:10.1371/journal.pbio.1001715

Sara C Cloutier, Siwen Wang + Show 4 more

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https://doi.org/10.1371/journal.pbio.1001715

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Abstract

Author SummaryLong noncoding RNAs (lncRNAs) are a recently identified class of molecules that regulate the expression of protein-coding genes through a number of mechanisms, some of them poorly characterized. The GAL gene cluster of the yeast Saccharomyces cerevisiae encodes a series of three inducible genes that are turned on or off by the presence or absence of specific carbon sources in the environment. Previous studies have documented the presence of two lncRNAs—GAL10 and GAL10s—encoded by genes that overlap the GAL cluster. We have now uncovered a role for both these lncRNAs in promoting the activation of the GAL genes when they are released from repressive conditions. This activation occurs at the kinetic level, through more rapid recruitment of RNA polymerase II and decreased association of the co-repressor, Cyc8. Under normal conditions, but also especially when they are stabilized and their levels are up-regulated, these GAL lncRNAs promote faster GAL gene activation. We suggest that these lncRNA molecules poise inducible genes for quick response to extracellular cues, triggering a faster switch in transcriptional programs.

Highlights

Essential cellular processes, such as growth, organ development, and differentiation, require precise spatial and temporal control of gene expression
Previous studies have documented the presence of two long noncoding RNA (lncRNA)—GAL10 and GAL10s—encoded by genes that overlap the galactose metabolic gene (GAL) cluster
We have uncovered a role for both these lncRNAs in promoting the activation of the GAL genes when they are released from repressive conditions

Summary

Introduction

Essential cellular processes, such as growth, organ development, and differentiation, require precise spatial and temporal control of gene expression. Other lncRNAs, appear to function solely through their synthesis, whereby the act of transcription alters the chromatin structure of a targeted gene promoter [14,15,16]. Many mammalian lncRNAs are associated with genes that require precise temporal control of initiation to facilitate proper cell growth and differentiation [9,13,18,19,20,21,22,23]. This suggests that these molecules may control the timing of gene expression in response to specific signals

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