Comparative Network Analysis Reveals That Tissue Specificity and Gene Function Are Important Factors Influencing the Mode of Expression Evolution in Arabidopsis and Rice  

Abstract

Microarray experiments have yielded massive amounts of expression information measured under various conditions for the model species Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa). Expression compendia grouping multiple experiments make it possible to define correlated gene expression patterns within one species and to study how expression has evolved between species. We developed a robust framework to measure expression context conservation (ECC) and found, by analyzing 4,630 pairs of orthologous Arabidopsis and rice genes, that 77% showed conserved coexpression. Examples of nonconserved ECC categories suggested a link between regulatory evolution and environmental adaptations and included genes involved in signal transduction, response to different abiotic stresses, and hormone stimuli. To identify genomic features that influence expression evolution, we analyzed the relationship between ECC, tissue specificity, and protein evolution. Tissue-specific genes showed higher expression conservation compared with broadly expressed genes but were fast evolving at the protein level. No significant correlation was found between protein and expression evolution, implying that both modes of gene evolution are not strongly coupled in plants. By integration of cis-regulatory elements, many ECC conserved genes were significantly enriched for shared DNA motifs, hinting at the conservation of ancestral regulatory interactions in both model species. Surprisingly, for several tissue-specific genes, patterns of concerted network evolution were observed, unveiling conserved coexpression in the absence of conservation of tissue specificity. These findings demonstrate that orthologs inferred through sequence similarity in many cases do not share similar biological functions and highlight the importance of incorporating expression information when comparing genes across species.

Systematic Identification of Functional Plant Modules through the Integration of Complementary Data Sources

“…Although it is currently unclear whether this pattern holds for all genes, this estimate provides an experimental indication that complex regulation, as indicated by our modules, will be true for some genes. The variation in regulatory complexity for different GO-BP slim categories confirms that function, apart from other factors, is an important element contributing to a gene's regulation (Freeling et al, 2007;Movahedi et al, 2011).…”

“…These networks were built combining expression and PPI data with sequence data (Kourmpetis et al, 2011), genetic and physical interaction data (Warde-Farley et al, 2010), phylogenetic profiles and gene location (Bradford et al, 2010), and the integration of functional genomics, proteomics, and comparative genomics data sets (Lee et al, 2010). Apart from studying gene modules in one species, recent studies have applied comparisons across species to identify conserved gene coexpression in plants (Ficklin and Feltus, 2011;Movahedi et al, 2011;Mutwil et al, 2011). The analysis of coexpression networks between more distantly related species exploits the assumption that predicted gene function associations, occurring by chance within one organism, will not be conserved in a multispecies context.…”

Characteristics and Significance of Intergenic Polyadenylated RNA Transcription in Arabidopsis

“…In terms of translation, ITFs behave similarly to pseudogenes and transposons. Previous studies have suggested that the breadth of expression as well as the level of expression can be considered as proxy indicators of functionality (Nuzhdin et al, 2004;Subramanian and Kumar, 2004;Movahedi et al, 2011). However, genes can have highly specific expression and/or low expression levels.…”

Dissecting Plant Genomes with the PLAZA Comparative Genomics Platform

“…The reliability of the different orthology predictions was scored with the ECC score (Movahedi et al, 2011). ECC compared the expression profile conservation between two species by a statistical framework evaluating shared homologous relationships between coexpressed genes.…”

“…As expected, reconciled phylogenetic trees only provided orthology information for 18,415 Arabidopsis genes. To evaluate the quality of these predictions, the percentage of orthologous gene pairs with conserved expression was determined by using the expression context conservation (ECC; Movahedi et al, 2011). The expression context was based on the expression similarity between a query gene and all other genes in that species (gene-centric coexpression cluster).…”