Decrease in Purifying Selection Pressures on Wheat Homoeologous Genes: Tetraploidization vs Hexaploidization

Abstract

A series of polyploidizations in higher-order polyploids is the main event affecting the gene contents in a genome, and this is frequently observed in domesticated plants. Each polyploidization event is expected to lead to functional divergence because of the associated decrease in the selection pressures on the duplicated genes, but it is unclear whether the initial tetraploidization or the subsequent higher-order polyploidization has a greater evolutionary impact on the duplicated genes. To address this uncertainty, we focused on the Triticum-Aegilops complex lineage and compared the selection pressures before and after the tetraploidization and hexaploidization events. The results indicated that while both events decreased the selection pressures on homoeologous gene pairs (compared with the selection pressures on their ancestral diploid and tetraploid orthologous genes), the initial tetraploidization had a greater impact on the selection pressures on homoeologous gene pairs than the subsequent hexaploidization. This was supported by the analyzed expression patterns. Surprisingly, the decreases in the selection pressures on these homoeologous genes were independent of the existence of in-paralogs within the same subgenome. This result suggests that unique functions are maintained in the homoeologous genes, including the functions that are unlikely to be preserved in duplicate gene pairs derived from other duplication mechanisms. We also revealed their unique functions were different between the tetra- and hexaploidization (e.g., Reproductive system and chromosome segregation processes). The findings of this study imply that the substantial number of gene pairs resulting from multiple allopolyploidization events, especially the initial tetraploidization, may have been a unique source of functional divergence.