Comparative network analysis reveals that tissue specificity and gene function are important factors influencing the mode of expression evolution in Arabidopsis and rice

¹ Department of Plant Systems Biology, VIB, Technologiepark 927, B-9052 Gent, Belgium

² Department of Molecular Genetics, Ghent University Technologiepark 927, B-9052 Gent, Belgium

^*Corresponding author, E-mail: klaas.vandepoele@psb.vib-ugent.be

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 4630 pairs of orthologous Arabidopsis and rice genes, that 77% showed conserved coexpression. Examples of non-conserved 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 to broadly expressed genes but are 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.

Supplementary Data

• Arabidopsis expression clusters (download tab-delimited compressed file)
• Rice expression clusters (download tab-delimited compressed file)
• Arabidopsis:Rice orthologous families (download tab-delimited compressed file)
• ECC results 4630 orthologous Arabidopsis:Rice gene pairs (download excel sheet)