Abstract
The trypanosome genome is characterized by RNA polymerase II-driven polycistronic transcription of protein-coding genes. Ten to hundreds of genes are co-transcribed from a single promoter; thus, selective regulation of individual genes via initiation is impossible. However, selective responses to external stimuli occur and post-transcriptional mechanisms are thought to account for all temporal gene expression patterns. We show that genes encoding mRNAs that are differentially regulated during the heat-shock response are selectively positioned in polycistronic transcription units; downregulated genes are close to transcription initiation sites and upregulated genes are distant. We demonstrate that the position of a reporter gene within a transcription unit is sufficient to reproduce this effect. Analysis of gene ontology annotations reveals that positional bias is not restricted to stress–response genes and that there is a genome-wide organization based on proximity to transcription initiation sites. Furthermore, we show that the relative abundance of mRNAs at different time points in the cell division cycle is dependent on the location of the corresponding genes to transcription initiation sites. This work provides evidence that the genome in trypanosomes is organized to facilitate co-coordinated temporal control of gene expression in the absence of selective promoters.
Highlights
The trypanosomatids are a monophyletic group of unicellular eukaryotes [1,2]
Linked endonucleolytic cleavage and polyadenylation of the upstream mRNA complete the maturation process. This mechanism of gene expression is reflected in the structure and organization of the genome, where protein-coding genes are densely packed in polycistronically transcribed tandem arrays containing tens to hundreds of genes with greater than 50 per cent of the nucleotide sequence of the array present in mature mRNAs [6,7,8]
A previous analysis of the heat-shock response in procyclic form Trypanosoma brucei identified 1058 mRNAs whose abundance changed in response to heat shock [27]
Summary
The trypanosomatids are a monophyletic group of unicellular eukaryotes [1,2]. The majority of characterized species are pathogenic, and collectively they inhabit a diverse range of hosts from coconut palms [3] to kangaroos [4], several& 2012 The Authors. Co-transcriptional processing to individual monocistronic mRNAs is mediated by trans-splicing of a 39-nucleotidecapped exon to the 50 end of all protein-coding genes. Linked endonucleolytic cleavage and polyadenylation of the upstream mRNA complete the maturation process This mechanism of gene expression is reflected in the structure and organization of the genome, where protein-coding genes are densely packed in polycistronically transcribed tandem arrays containing tens to hundreds of genes with greater than 50 per cent of the nucleotide sequence of the array present in mature mRNAs [6,7,8]. Many diverse eukaryotes (including appendicularia, ascidians, cnidarians, dinoflagellates, nematodes, platyhelminthes and rotifers) partially or entirely rely on this form of transcription for expression of their protein-coding genes [9,10,11,12,13]
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