Function relaxation followed by diversifying selection after whole-genome duplication in flowering plants

Episodes of whole-genome duplication (WGD) followed by gene loss dominate the evolutionary history of flowering plants. Despite the importance of understanding gene evolution following WGD, little is known about the evolutionary dynamics of this process. In this study, we analyzed duplicated genes from three WGD events in the Arabidopsis (Arabidopsis thaliana) lineage using multiple data types. Most duplicated genes that have survived from the most recent WGD (α) are under purifying selection in modern Arabidopsis populations. Using the number of identified protein-protein interactions as a proxy for functional divergence, approximately 92.7% of α-duplicated genes were diverged in function from one another in modern Arabidopsis populations, indicating that their preservation is no longer explicable by dosage balance. Dosage-balanced retention declines with antiquity of duplication: 24.1% of α-duplicated gene pairs in Arabidopsis remain in dosage balance with interacting partners, versus 12.9% and 9.4% for the earlier β-duplication and γ-triplication. GO-slim (a cut-down version of gene ontologies) terms reinforce evidence from protein-protein interactions, showing that the putatively diverged gene pairs are adapted to different cellular components. We identified a group of α-duplicated genes that show higher than average single-nucleotide polymorphism density, indicating that a period of positive selection, potentially driving functional divergence, may have preceded the current phase of purifying selection. We propose three possible paths for the evolution of duplicated genes following WGD.