Evolution of gene function and regulatory control after whole-genome duplication: Comparative analyses in vertebrates

Abstract

The significance of whole-genome duplications (WGD) for vertebrate evolution remains controversial, in part because the mechanisms by which WGD contributed to functional evolution or speciation are still incompletely characterized. Fish genomes provide an ideal context in which to examine the consequences of WGD, because the teleost lineage experienced an additional WGD soon after divergence from tetrapods and because five teleost genomes are available for comparative analysis. Here we present an integrated approach to characterize these post-duplication genomes based on genome-scale synteny, phylogenetic, temporal, and spatial gene expression and on protein sequence data. A minimum of 3%-4% of protein-coding loci have been retained in two copies in each of the five fish genomes, and many of these duplicates are key developmental genes that function as transcription factors or signaling molecules. Almost all duplicate gene pairs we examined have diverged in spatial and/or temporal expression during embryogenesis. A quarter of duplicate pairs have diverged in function via the acquisition of novel protein domains or via changes in the subcellular localization of their encoded proteins. We compared the spatial expression and protein domain architecture of zebrafish WGD-duplicates to those of their single mouse ortholog and found many examples supporting a model of neofunctionalization. WGDduplicates have acquired novel protein domains more often than have single-copy genes. Post-WGD changes at the gene regulatory level were more common than changes at the protein level. We conclude that the most significant consequence of WGD for vertebrate evolution has been to enable more-specialized regulatory control of development via the acquisition of novel spatiotemporal expression domains. We find limited evidence that reciprocal gene loss led to reproductive isolation and speciation in this lineage.

Whole-genome duplication in teleost fishes and its evolutionary consequences

“…This is roughly in agreement with the first genome-wide, comparative analysis of five different fish species by Kassahn et al (Kassahn et al, 2009) These authors found that in all five species examined, 3-4% of the genes show strong evidence for having originated in the ancient TS-WGD. Due to the design of the study, this number is probably underestimating the real abundance of gene retention after TS-WGD, and can be considered a minimum estimate, as pointed out by the authors themselves.…”

How life changes itself: The Read–Write (RW) genome

“…The reason is that distributed genomic networks can undergo rapid modification and come to adopt encode novel functions without loss of the original functionality. This potential has contributed to the adaptation of signal transduction and other multicomponent systems to diverse cell and developmental functionalities [142][143][144][145].…”

Prevalent Role of Gene Features in Determining Evolutionary Fates of Whole-Genome Duplication Duplicated Genes in Flowering Plants

“…Given that the expression data employed for sorghum and maize were measured by ESTs, the observed subfunctionalization of gene expression should be treated with caution, and further analyses are needed. In a recent study, analyses of vertebrate WGD events showed that about 24% of the ohnologs encoded proteins that differed in domain architecture and/or subcellular localization (Kassahn et al, 2009). The usefulness of this analysis would be helpful to detect signatures of subfunctionalization at the sequence level without the lack of functional data or protein structure in many of our analyzed genomes and data sets.…”

“…Sémon and Wolfe (2008) suggested that subfunctionalization might play a prevalent role in both the initial preservation and long-term evolution of WGD duplicated genes. Another recent study with several vertebrate genomes supported that neofunctionalization is more prevalent (Kassahn et al, 2009). However, Freeling (2008, 2009) argued that if subfunctionalization or neofunctionalization was dominant after WGDs, then functional classes overretained for WGD duplicates might also be enriched for duplicates derived from SSDs, due to the similar evolutionary forces operating on them.…”

“…Besides the investigation of gene features related to the evolution of WGD duplicated genes, great efforts have been made to elucidate which evolutionary models may apply to WGD duplicates, such as subfunctionalization, neofunctionalization, dosage balance, and beneficial selection for higher dosage (Seoighe and Wolfe, 1999;Papp et al, 2003;Sémon and Wolfe, 2008;Kassahn et al, 2009). Sémon and Wolfe (2008) suggested that subfunctionalization might play a prevalent role in both the initial preservation and long-term evolution of WGD duplicated genes.…”