Life and Death in the Paleopolyploid Genome: Contrasting Patterns of Duplicate Gene Evolution in Populus

Gene duplication provides the primary source of novel gene content across diverse taxa, and whole genome duplications (WGD) have recurrently shaped the evolution of most angiosperm lineages. Following duplication, a diploid state is often restored through a process of fractionation, during which many of the duplicate genes are lost. We are studying duplicate gene evolution in Populus, in which approximately 2/3 of the whole genome duplicates have been deleted or pseudogenized. We have found that the functional composition strongly differs between genes preserved from WGD and those that proliferate through small-scale, tandem duplications, with a bias toward genes that should have high connectivity in regulatory networks in WGD. This observation is consistent with the Gene Balance hypothesis, which posits that selection for the maintenance of a stoichiometric balance between interacting genes drives retention and loss of duplicates. By contrast, the subfunctionalization hypothesis posits that duplicate preservation is driven by neutrally accumulating degenerative mutations. Based on whole genome microarray analysis across a diversity of tissues, we show that approximately half of the duplicate genes have diverged in a manner concordant with a random subfunctionalization process, while the other half are more conserved than expected by chance, possibly consistent with selection for gene balance. Subsequent analyses will focus on using comparative genomics to determine rates and patterns of pseudogenization, and to identify regulatory elements responsible for subfunctionalization, thereby providing some insights into the mysterious yet fundamentally important evolutionary trajectories of whole genome duplications.