The budding yeast rRNA and ribosome biosynthesis (RRB) regulon contains over 200 genes

Abstract

The ribosome biogenesis pathway constitutes one of the major metabolic obligations for a dividing yeast cell and it depends upon the activity of hundreds of gene products to produce the necessary rRNA and ribosomal protein components. Previously, we reported that a set of 65 S. cerevisiae genes that function in the rRNA biosynthesis pathway are transcriptionally co-regulated as cells pass through a variety of physiological transitions. By analysing multiple microarray-based transcriptional datasets, we have extended that study and now suggest that the ribosomal and rRNA biosynthesis regulon contains over 200 genes. This regulon is distinct from the set of ribosomal protein genes, and the promoters of the expanded RRB gene set are highly enriched for the PAC and RRPE motifs. Since a similar pattern of organization and gene regulation can be recognized in C. albicans, the RRB regulon appears to be a conserved, extensive, and metabolically important group of genes.

Protein kinase A and TORC1 activate genes for ribosomal biogenesis by inactivating repressors encoded by Dot6 and its homolog Tod6

“…The promoters of Ribi genes are highly enriched in PAC motifs (7,12,13). The Saccharomyces Genome Database currently annotates 303 nonribosomal protein genes in the functional category of ribosome biogenesis, and 199 of these overlap with the 647 genes whose promoters contain one or more PAC sites (P Ͻ 10 Ϫ190 ).…”

“…Moreover, another Ϸ300 genes encoding nonribosomal proteins are involved in various aspects of ribosome assembly and translational capacity (the ribosome biogenesis, or Ribi, regulon): RNA polymerases I and III subunits, tRNA synthetases, rRNA processing and modifying enzymes, translation factors, etc. (6,7). Synthesis of the translation machinery is very energetically expensive to the cell.…”

“…Ribi gene promoters are enriched for RNA polymerases A (I) and C (III) (PAC), and ribosomal RNA-processing element (RRPE) motifs in specific orientation to each other and to the transcriptional start site (7,12,13). The split finger transcription factor Sfp1 has been implicated in Ribi gene regulation: loss of Sfp1 results in reduced expression of Ribi genes, whereas induction of Sfp1 results in a rapid activation of the Ribi regulon (13).…”

Chromatin-dependent Transcription Factor Accessibility Rather than Nucleosome Remodeling Predominates during Global Transcriptional Restructuring in Saccharomyces cerevisiae

“…Promoters of the glucose-induced ribosomal biogenesis genes are highly enriched for RRPE and PAC motifs (Beer and Tavazoie, 2004;Jorgensen et al, 2004;Wade et al, 2006). Quite strikingly, in the promoters of those genes containing a PAC or RRPE motif (labeled Motif B in Figure 6) that were subsequently induced by glucose addition, the motifs were significantly more exposed than they were in those genes that were subsequently repressed or remained unchanged upon glucose addition, suggesting that likely physiologically relevant occurrences of RRPE/PAC motifs may be free of nucleosomes and accessible, whereas likely spurious instances of the RRPE/PAC motifs in promoters of repressed or unchanged genes are more likely to be contained within nucleosomes and perhaps inaccessible.…”

Two by Two: Co-Regulating Adjacent Gene Pairs in Yeast and Beyond

“…We found that the promoters of the RRB genes were enriched for the PAC and RRPE promoter motifs, and substitutions in these motifs disturbed the regulated expression of candidate RRB genes in vivo [5]. By analyzing genome-wide expression profiles, and cross referencing with the presence of the conserved promoter motifs, we were able to suggest that the RRB regulon contained some 200 members, even though many of the genes had at the time, no ascribed function [5,6].These predictions have turned out to be fairly accurate, as since then some 90% of the unknown members have been subsequently identified as contributing towards ribosome and rRNA biogenesis. The factors that recognize the PAC and RRPE motifs have also been subsequently identified (the Stb3 and Tod6/Dot6 proteins respectively), and they have been shown to play key roles in RRB gene regulation [7].…”