Organ Evolution in Angiosperms Driven by Correlated Divergences of Gene Sequences and Expression Patterns

The evolution of a species involves changes in its genome and its transcriptome. Divergence in expression patterns may be more important than divergence in sequences for determining phenotypic changes, particularly among closely related species. We examined the relationships between organ evolution, sequence evolution, and expression evolution in Arabidopsis thaliana, rice (Oryza sativa), and maize (Zea mays). We found correlated divergence of gene sequences and expression patterns, with distinct divergence rates that depend on the organ types in which a gene is expressed. For instance, genes specifically expressed in reproductive organs (i.e., stamen) evolve more quickly than those specifically expressed in vegetative organs (e.g., root). The different rates in organ evolution may be due to different degrees of functional constraint associated with the different physiological functions of plant organs. Additionally, the evolutionary rate of a gene sequence is correlated with the breadth of its expression in terms of the number of tissues, the number of coregulation modules, and the number of species in which the gene is expressed, as well as the number of genes with which it may interact. This linkage supports the hypothesis that constitutively expressed genes may experience higher levels of functional constraint accumulated from multiple tissues than do tissue-specific genes.