Abstract

BackgroundCoordinated cell growth and development requires that cells regulate the expression of large sets of genes in an appropriate manner, and one of the most complex and metabolically demanding pathways that cells must manage is that of ribosome biogenesis. Ribosome biosynthesis depends upon the activity of hundreds of gene products, and it is subject to extensive regulation in response to changing cellular conditions. We previously described an unusual property of the genes that are involved in ribosome biogenesis in yeast; a significant fraction of the genes exist on the chromosomes as immediately adjacent gene pairs. The incidence of gene pairing can be as high as 24% in some species, and the gene pairs are found in all of the possible tandem, divergent, and convergent orientations.ResultsWe investigated co-regulated gene sets in S. cerevisiae beyond those related to ribosome biogenesis, and found that a number of these regulons, including those involved in DNA metabolism, heat shock, and the response to cellular stressors were also significantly enriched for adjacent gene pairs. We found that as a whole, adjacent gene pairs were more tightly co-regulated than unpaired genes, and that the specific gene pairing relationships that were most widely conserved across divergent fungal lineages were correlated with those genes that exhibited the highest levels of transcription. Finally, we investigated the gene positions of ribosome related genes across a widely divergent set of eukaryotes, and found a significant level of adjacent gene pairing well beyond yeast species.ConclusionWhile it has long been understood that there are connections between genomic organization and transcriptional regulation, this study reveals that the strategy of organizing genes from related, co-regulated pathways into pairs of immediately adjacent genes is widespread, evolutionarily conserved, and functionally significant.

Highlights

  • Coordinated cell growth and development requires that cells regulate the expression of large sets of genes in an appropriate manner, and one of the most complex and metabolically demanding pathways that cells must manage is that of ribosome biogenesis

  • Gene pairing is associated with tighter transcriptional co-regulation within the rRNA biosynthesis (RRB) and ribosomal proteins (RPs) regulons In our previous analysis of the genes that are involved in ribosome biogenesis in S. cerevisiae, we noted that some 13% of the RP genes, and 15% of the RRB genes are located on the chromosomes as immediately adjacent gene pairs

  • To investigate what functional significance may be associated with this high degree of adjacent gene pairing, we investigated the transcriptional response of the RRB and RP genes following a 37°C heat-shock [3]

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Summary

Introduction

Coordinated cell growth and development requires that cells regulate the expression of large sets of genes in an appropriate manner, and one of the most complex and metabolically demanding pathways that cells must manage is that of ribosome biogenesis. Ribosome biosynthesis depends upon the activity of hundreds of gene products, and it is subject to extensive regulation in response to changing cellular conditions. The localization of genes to particular sub-nuclear compartments can change quickly in response to environmental cues, where the activation of a gene can result in its re-localization to the nuclear periphery, allowing for coordination of transcription with processing and nuclear export [9]

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