Abstract
Regulation of gene expression via specific cis-regulatory promoter elements has evolved in cellular organisms as a major adaptive mechanism to respond to environmental change. Assuming a simple model of transcriptional regulation, genes that are differentially expressed in response to a large number of different external stimuli should harbor more distinct regulatory elements in their upstream regions than do genes that only respond to few environmental challenges. We tested this hypothesis in Arabidopsis thaliana using the compendium of gene expression profiling data available in AtGenExpress and known cis-element motifs mapped to upstream gene promoter regions and studied the relation of the observed breadth of differential gene expression response with several fundamental genome architectural properties. We observed highly significant positive correlations between the density of cis-elements in upstream regions and the number of conditions in which a gene was differentially regulated. The correlation was most pronounced in regions immediately upstream of the transcription start sites. Multistimuli response genes were observed to be associated with significantly longer upstream intergenic regions, retain more paralogs in the Arabidopsis genome, are shorter, have fewer introns, and are more likely to contain TATA-box motifs in their promoters. In abiotic stress time series data, multistimuli response genes were found to be overrepresented among early-responding genes. Genes involved in the regulation of transcription, stress response, and signaling processes were observed to possess the greatest regulatory capacity. Our results suggest that greater gene expression regulatory complexity appears to be encoded by an increased density of cis-regulatory elements and provide further evidence for an evolutionary adaptation of the regulatory code at the genomic layout level. Larger intergenic spaces preceding multistimuli response genes may have evolved to allow greater regulatory gene expression potential.
Highlights
The regulation of gene expression has evolved in cellular organisms as a major adaptive mechanism to respond to environmental changes [1,2,3,4,5]
This process is mediated via molecular switches, so-called regulatory elements, generally located in the genomic region adjacent to the gene they control, the gene promoter
Specific proteins bind to such regulatory elements, thereby turning on or off the associated genes. As this molecular response is often specific to the external signal, genes that respond to a large number of different external stimuli should harbor more distinct regulatory elements in their promoter regions than should genes responding only to few environmental challenges
Summary
The regulation of gene expression has evolved in cellular organisms as a major adaptive mechanism to respond to environmental changes [1,2,3,4,5]. The induction or repression of particular genes in response to specific environmental challenges is primarily controlled by the recognition and binding of transcriptional regulator proteins (transcription factors) to cis-regulatory elements constituted by short DNA sequence motif sites located in the upstream regions of genes [11,12,13]. Under the simplest scenario of transcriptional regulation, distinct external challenges are matched by specific cognate regulatory sites in upstream regulatory regions of genes that have evolved to respond to the particular perturbation. Genes that are differentially expressed in response to a large number of different external stimuli (multistimuli response genes) are expected to contain more distinct cis-regulatory elements in their upstream regions than are genes that respond to only few environmental cues. The association of Editor: Yoshihide Hayashizaki, RIKEN Genomic Sciences Center, Japan
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