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The regulatory code for transcriptional response diversity and its relation to genome structural properties in A. thaliana.

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.

SUBMITTER: Walther D

PROVIDER: S-EPMC1796623 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundLow temperature leads to major crop losses every year. Although several studies have been conducted focusing on diversity of cold tolerance level in multiple phenotypically divergent Arabidopsis thaliana (A. thaliana) ecotypes, genome-scale molecular understanding is still lacking.ResultsIn this study, we report genome-scale transcript response diversity of 10 A. thaliana ecotypes originating from different geographical locations to non-freezing cold stress (10°C). To analyze the transcriptional response diversity, we initially compared transcriptome changes in all 10 ecotypes using Arabidopsis NimbleGen ATH6 microarrays. In total 6061 transcripts were significantly cold regulated (p < 0.01) in 10 ecotypes, including 498 transcription factors and 315 transposable elements. The majority of the transcripts (75%) showed ecotype specific expression pattern. By using sequence data available from Arabidopsis thaliana 1001 genome project, we further investigated sequence polymorphisms in the core cold stress regulon genes. Significant numbers of non-synonymous amino acid changes were observed in the coding region of the CBF regulon genes. Considering the limited knowledge about regulatory interactions between transcription factors and their target genes in the model plant A. thaliana, we have adopted a powerful systems genetics approach- Network Component Analysis (NCA) to construct an in-silico transcriptional regulatory network model during response to cold stress. The resulting regulatory network contained 1,275 nodes and 7,720 connections, with 178 transcription factors and 1,331 target genes.ConclusionsA. thaliana ecotypes exhibit considerable variation in transcriptome level responses to non-freezing cold stress treatment. Ecotype specific transcripts and related gene ontology (GO) categories were identified to delineate natural variation of cold stress regulated differential gene expression in the model plant A. thaliana. The predicted regulatory network model was able to identify new ecotype specific transcription factors and their regulatory interactions, which might be crucial for their local geographic adaptation to cold temperature. Additionally, since the approach presented here is general, it could be adapted to study networks regulating biological process in any biological systems.

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The regulatory code for transcriptional response diversity and its relation to genome structural properties in A. thaliana.

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