Abstract
The resource intensive process of accurate ribosome synthesis is essential for cell viability in all organisms. Ribosome synthesis regulation centers on RNA polymerase I (pol I) transcription of a 35S rRNA precursor that is processed into the mature 18S, 5.8S and 25S rRNAs. During nutrient deprivation or stress, pol I synthesis of rRNA is dramatically reduced. Conversely, chronic stress such as mitochondrial dysfunction induces RNA polymerase II (pol II) to transcribe functional rRNA using an evolutionarily conserved cryptic pol II rDNA promoter suggesting a universal phenomenon. However, this polymerase switches and its role in regulation of rRNA synthesis remain unclear. In this paper, we demonstrate that extended nitrogen deprivation induces the polymerase switch via components of the environmental stress response. We further show that the switch is repressed by Sch9 and activated by the stress kinase Rim15. Like stress-induced genes, the switch requires not only pol II transcription machinery, including the mediator, but also requires the HDAC, Rpd3 and stress transcription factor Hsf1. The current work shows that the constitutive allele, Hsf1PO4* displays elevated levels of induction in non-stress conditions while binding to a conserved site in the pol II rDNA promoter upstream of the pol I promoter. Whether the polymerase switch serves to provide rRNA when pol I transcription is inhibited or fine-tunes pol I initiation via RNA interactions is yet to be determined. Identifying the underlying mechanism for this evolutionary conserved phenomenon will help understand the mechanism of pol II rRNA synthesis and its role in stress adaptation.
Highlights
Ribosomal synthesis is the most resource intensive cellular process, and cell viability is highly dependent on the precise production and assembly of ribosomes
We demonstrate that the processes that prohibit pol I pre-initiation complex (PIC) formation triggers Heat Shock Transcription Factor 1 (Hsf1) mediated synthesis of rRNA by RNA polymerase II
To investigate the hypothesis that polymerase II (pol II) synthesizes rRNA during stress conditions other than mitochondrial dysfunction, we inspected the pol II rDNA promoter for putative transcription factor binding sites using YeTFaSCo (De Boer and Hughes 2011)
Summary
Ribosomal synthesis is the most resource intensive cellular process, and cell viability is highly dependent on the precise production and assembly of ribosomes. Ribosome production is tightly linked to growth rate and the need for protein synthesis (Kief and Warner 1981) with RNA polymerase I (pol I) transcription of rRNA being the rate limiting step (Laferté et al 2006; Chedin et al 2007). We demonstrate that the processes that prohibit pol I PIC formation triggers Heat Shock Transcription Factor 1 (Hsf1) mediated synthesis of rRNA by RNA polymerase II (pol II). This polymerase switch employs factors required for general stress response in yeast classifying pol II rRNA synthesis as a stress response. The synthesis of rRNA by pol II is evolutionarily conserved suggesting that it contributes to the regulation of rRNA synthesis, in general
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