Abstract
The evolution of genes and genomes after polyploidization has been the subject of extensive studies in evolutionary biology and plant sciences. While a significant number of duplicated genes are rapidly removed during a process called fractionation, which operates after the whole-genome duplication (WGD), another considerable number of genes are retained preferentially, leading to the phenomenon of biased gene retention. However, the evolutionary mechanisms underlying gene retention after WGD remain largely unknown. Through genome-wide analyses of sequence and functional data, we comprehensively investigated the relationships between gene features and the retention probability of duplicated genes after WGDs in six plant genomes, Arabidopsis (Arabidopsis thaliana), poplar (Populus trichocarpa), soybean (Glycine max), rice (Oryza sativa), sorghum (Sorghum bicolor), and maize (Zea mays). The results showed that multiple gene features were correlated with the probability of gene retention. Using a logistic regression model based on principal component analysis, we resolved evolutionary rate, structural complexity, and GC3 content as the three major contributors to gene retention. Cluster analysis of these features further classified retained genes into three distinct groups in terms of gene features and evolutionary behaviors. Type I genes are more prone to be selected by dosage balance; type II genes are possibly subject to subfunctionalization; and type III genes may serve as potential targets for neofunctionalization. This study highlights that gene features are able to act jointly as primary forces when determining the retention and evolution of WGD-derived duplicated genes in flowering plants. These findings thus may help to provide a resolution to the debate on different evolutionary models of gene fates after WGDs.
Highlights
The evolution of genes and genomes after polyploidization has been the subject of extensive studies in evolutionary biology and plant sciences
The evolutionary history of whole-genome duplication (WGD) has been extensively characterized in the six plant genomes under investigation (Bowers et al, 2003; Paterson et al, 2004; Tuskan et al, 2006; Schnable et al, 2009; Schmutz et al, 2010)
This study aimed to examine the patterns of fractionation after WGDs in general across divergent plant lineages; all six genomes, Arabidopsis, poplar, soybean, rice, sorghum, and maize (Supplemental Table S1), were reanalyzed under a similar framework to minimize variations caused by methodology discrepancy
Summary
The evolution of genes and genomes after polyploidization has been the subject of extensive studies in evolutionary biology and plant sciences. This study highlights that gene features are able to act jointly as primary forces when determining the retention and evolution of WGD-derived duplicated genes in flowering plants These findings may help to provide a resolution to the debate on different evolutionary models of gene fates after WGDs. Polyploidy, known as the whole-genome duplication (WGD), plays a significant role in plant diversification and evolution (Otto and Whitton, 2000; Soltis et al, 2009). Studies on the Compositae (Asteraceae) lineage showed that duplicated genes generated by WGD were significantly enriched for genes associated with structural components or cellular organization, and regulatory and developmental genes such as transcription factors were significantly underrepresented This pattern was almost consistent in all Compositae species investigated (Barker et al, 2008). Exploring evolutionary models applied to WGD events is still an open question to evolutionary biologists
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