Gene function is a driver of signaling pathway evolution following whole genome 5 duplication

Abstract

The genome of many plant and animal species are heavily influenced by ancestral whole genome duplication (WGD) events. These events transform the regulation and function of gene networks, yet the evolutionary forces at work on duplicated genomes are not fully understood. Genes involved in cell surface signaling pathways are commonly retained following WGD. To understand the mechanisms driving functional evolution of duplicated cell signaling pathways, we performed the activin receptor signaling pathway in rainbow trout (RBT). Rainbow trout are a model salmonid species that exhibit a duplicated genome as a result of an ancestral WGD that occurred in all teleost fish, and a second more recent WGD found in salmonid fishes. This makes RBT a powerful system for studying ohnolog evolution in a single species. We observed that regulation of the duplicated activin receptor signaling pathway is commonly driven by tissue-specific expression of inhibitors and ligands along with the subfunctionalization of ligand ohnologs. Evidence suggests that for inhibitors and R-Smad signaling molecules, there is ongoing pressure to establish a single copy state which may be driven, in part, by regulatory suppression of select ohnologs. The core transmembrane receptors and Co-Smad signaling cascade members are high duplicated yet exhibit contrasting expression dynamics where receptors tend to share expression across tissues while dominance of a single ohnolog is common for the Smad4, Co-Smad gene family. Our findings provide support for a generalized model where gene function and gene dosage have a complementary role in ohnolog evolution following WGD.