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. 2012:2012:276948.
doi: 10.1155/2012/276948. Epub 2012 Jan 12.

Regulation of ribosomal RNA production by RNA polymerase I: does elongation come first?

Benjamin Albert  1 , Jorge Perez-Fernandez, Isabelle Léger-Silvestre, Olivier Gadal
Affiliations

Regulation of ribosomal RNA production by RNA polymerase I: does elongation come first?

Benjamin Albert et al. Genet Res Int. 2012.

Abstract

Ribosomal RNA (rRNA) production represents the most active transcription in the cell. Synthesis of the large rRNA precursors (35-47S) can be achieved by up to 150 RNA polymerase I (Pol I) enzymes simultaneously transcribing each rRNA gene. In this paper, we present recent advances made in understanding the regulatory mechanisms that control elongation. Built-in Pol I elongation factors, such as Rpa34/Rpa49 in budding yeast and PAF53/CAST in humans, are instrumental to the extremely high rate of rRNA production per gene. rRNA elongation mechanisms are intrinsically linked to chromatin structure and to the higher-order organization of the rRNA genes (rDNA). Factors such as Hmo1 in yeast and UBF1 in humans are key players in rDNA chromatin structure in vivo. Finally, elongation factors known to regulate messengers RNA production by RNA polymerase II are also involved in rRNA production and work cooperatively with Rpa49 in vivo.

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Figures

Figure 1
Figure 1
Budding yeast cells and ribosome production. (a) Morphology of Saccharomyces cerevisiae cells after cryofixation and freeze substitution. Ribosomes are individually localized in the cytoplasm (see individual ribosomes detected in the zoomed region). In the nucleus, the nucleolus (No) is detected as a large electron-dense region compared with low electron density of the nucleoplasm (Np). (b) Morphology of the nucleolus. The nucleus appears outlined by a double envelope with pores, and the nucleolus is in close contact with the nuclear envelope. In the nucleolus, a dense fibrillar network is visible throughout the nucleolar volume. Granular components are dispersed throughout the rest of the nucleolus. (c) Visualization of active genes in rDNA. Using a mutant strain with a reduced number of rDNA copies (strain NOY1071; 25 rDNA copies), Miller spreading of total nucleolar DNA allowed single-gene analysis of rRNA genes. (d) Quantification of actively transcribed rDNA. Using high magnification, we can detect individual polymerases associated with nascent rRNA. Bars represent 500 nm.
Figure 2
Figure 2
Schematic representation of the Pol I transcription cycle. Simplified composition of the Pol I preinitiation complex (PIC) in (a) budding yeast and (b) human cells. The Pol I transcription cycle in budding yeast. (1) Recruitment of Rrn3/Pol I onto an rDNA promoter associated with the SL1 and UAF complex allows PIC formation. (2) Promoter escape and rRNA synthesis are coupled with cotranscriptional recruitment of the SSU processome. (3) Rrn3 dissociation is achieved by the formation of an adjacent PIC. Pol I subunits Rpa49 and Rpa43 from the adjacent polymerases promote Rrn3 release from the transcribing Pol I. (4) Pol I transcription of rRNA is coupled with nascent rRNA processing and termination. (5) Pol I holoenzyme is recycled by reassociation with Rrn3, an as yet uncharacterized regulatory process. Hmo1 function during elongation remains to be clarified, but is revealed by a tight genetic interaction with Pol I elongation mutant rpa49Δ (4 and 5).
Figure 3
Figure 3
Miller spreading of nontranscribed rDNA. Single-gene analysis of nontranscribed rRNA genes reveals nucleosomal (a) and nonnucleosomal (b) organization. Chromatin spreading (upper panel) and a schematic representation of rDNA spreading (lower panel) are shown from strain NOY1071, bearing 25 rDNA copies. Transcribed rRNA genes (green) are identified by high Pol I density, and nascent rRNAs are shown in black. Non-transcribed regions are depicted in red. Intergenic spaces (IGSs) are short (600 nm) and can be easily distinguished from inactive rRNA genes. Inactive genes are flanked by two IGSs. Due to the DNA wrapping around nucleosomes, nontranscribed genes associated with nucleosomes appear shorter (2,100 nm − (2 × 600 nm) = 900 nm) than genes devoid of nucleosomes (3,100 nm − (2 × 600) = 1,900 nm). With 15 nucleosomes detected and each wrapped around 146 bp, we observed a length reduction of approximately 1,000 nm.
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