Gene-Sharing Networks Reveal Organizing Principles of Transcriptomes in Arabidopsis and Other Multicellular Organisms

Abstract

Understanding tissue-related gene expression patterns can provide important insights into gene, tissue, and organ function. Transcriptome analyses often have focused on housekeeping or tissue-specific genes or on gene coexpression. However, by analyzing thousands of single-gene expression distributions in multiple tissues of Arabidopsis thaliana, rice (Oryza sativa), human (Homo sapiens), and mouse (Mus musculus), we found that these organisms primarily operate by gene sharing, a phenomenon where, in each organism, most genes exhibit a high expression level in a few key tissues. We designed an analytical pipeline to characterize this phenomenon and then derived Arabidopsis and human gene-sharing networks, in which tissues are connected solely based on the extent of shared preferentially expressed genes. The results show that tissues or cell types from the same organ system tend to group together to form network modules. Tissues that are in consecutive developmental stages or have common physiological functions are connected in these networks, revealing the importance of shared preferentially expressed genes in conferring specialized functions of each tissue type. The networks provide predictive power for each tissue type regarding gene functions of both known and heretofore unknown genes, as shown by the identification of four new genes with functions in guard cell and abscisic acid response. We provide a Web interface that enables, based on the extent of gene sharing, both prediction of tissue-related functions for any Arabidopsis gene of interest and predictions concerning the relatedness of tissues. Common gene-sharing patterns observed in the four model organisms suggest that gene sharing evolved as a fundamental organizing principle of gene expression in diverse multicellular eukaryotes.