Organ and Cell Type–Specific Complementary Expression Patterns and Regulatory Neofunctionalization between Duplicated Genes in Arabidopsis thaliana

Duplicated genes can contribute to the evolution of new functions and they are common in eukaryotic genomes. After duplication, genes can show divergence in their sequence and/or expression patterns. Qualitative complementary expression, or reciprocal expression, is when only one copy is expressed in some organ or tissue types and only the other copy is expressed in others, indicative of regulatory subfunctionalization or neofunctionalization. From analyses of two microarray data sets with 83 different organ types, developmental stages, and cell types in Arabidopsis thaliana, we determined that 30% of whole-genome duplicate pairs and 38% of tandem duplicate pairs show reciprocal expression patterns. We reconstructed the ancestral state of expression patterns to infer that considerably more cases of reciprocal expression resulted from gain of a new expression pattern (regulatory neofunctionalization) than from partitioning of ancestral expression patterns (regulatory subfunctionalization). Pollen was an especially common organ type for expression gain, resulting in contrasting expression of some duplicates in pollen. Many of the gene pairs with reciprocal expression showed asymmetric sequence rate evolution, consistent with neofunctionalization, and the more rapidly evolving copy often showed a more restricted expression pattern. A gene with reciprocal expression in pollen, involved in brassinosteroid signal transduction, has evolved more rapidly than its paralog, and it shows evidence for a new function in pollen. This study indicates the evolutionary importance of reciprocal expression patterns between gene duplicates, showing that they are common, often associated with regulatory neofunctionalization, and may be a factor allowing for retention and divergence of duplicated genes.