Evolutionary Fates and Dynamic Functionalization of Young Duplicate Genes in Arabidopsis Genomes.

Jun Wang,Feng Tao,Chuanzhu Fan,Nicholas C Marowsky

doi:10.1104/pp.16.01177

Abstract

Gene duplication is a primary means to generate genomic novelties, playing an essential role in speciation and adaptation. Particularly in plants, a high abundance of duplicate genes has been maintained for significantly long periods of evolutionary time. To address the manner in which young duplicate genes were derived primarily from small-scale gene duplication and preserved in plant genomes and to determine the underlying driving mechanisms, we generated transcriptomes to produce the expression profiles of five tissues in Arabidopsis thaliana and the closely related species Arabidopsis lyrata and Capsella rubella Based on the quantitative analysis metrics, we investigated the evolutionary processes of young duplicate genes in Arabidopsis. We determined that conservation, neofunctionalization, and specialization are three main evolutionary processes for Arabidopsis young duplicate genes. We explicitly demonstrated the dynamic functionalization of duplicate genes along the evolutionary time scale. Upon origination, duplicates tend to maintain their ancestral functions; but as they survive longer, they might be likely to develop distinct and novel functions. The temporal evolutionary processes and functionalization of plant duplicate genes are associated with their ancestral functions, dynamic DNA methylation levels, and histone modification abundances. Furthermore, duplicate genes tend to be initially expressed in pollen and then to gain more interaction partners over time. Altogether, our study provides novel insights into the dynamic retention processes of young duplicate genes in plant genomes.

Highlights

Gene duplication, which generates extra copies from ancestral genes, can provide raw materials for developing new functions and is one major means of contributing to the evolution of genomic novelty (Ohno, 1970; Ohta, 1989; Force et al, 1999; Lynch and Conery, 2000; Conant and Wolfe, 2008; Freeling, 2009; Kaessmann et al, 2009; Chen et al, 2013)
We identified 187 A. thaliana species-specific duplicate gene pairs that originated fewer than 5 MYA, and 58 Arabidopsis genus-specific duplicate gene pairs that originated after Arabidopsis split from C. rubella and before the divergence of A
192 conservation, 104 neofunctionalization, and 158 specialization cases were classified for the species-specific paralogs. 19 conservation, 23 neofunctionalization, and 36 specialization cases were classified for the genus-specific paralogs (Table 1). These results suggest that conservation, neofunctionalization, and specialization are the three main evolutionary processes of young duplicate genes in Arabidopsis

Summary

Introduction

Gene duplication, which generates extra copies from ancestral genes, can provide raw materials for developing new functions and is one major means of contributing to the evolution of genomic novelty (Ohno, 1970; Ohta, 1989; Force et al, 1999; Lynch and Conery, 2000; Conant and Wolfe, 2008; Freeling, 2009; Kaessmann et al, 2009; Chen et al, 2013). A set of analysis metrics was recently developed to quantitatively distinguish the four evolutionary trajectories of gene duplication by applying a phylogenetic comparison of the transcriptomic data of closely related Drosophila and mammal species (Assis and Bachtrog, 2013, 2015). Using expression profiles as proxies for function, the expression distances of two duplicate genes in Drosophila and mammal species to their ancestral gene in outgroup species were compared with that of single-copy genes to their outgroup orthologous genes (Assis and Bachtrog, 2013, 2015). These analysis metrics provide a valuable resource to study the evolutionary processes of preserving duplicate genes in other species. By taking advantage of the aforementioned phylogenetic approaches, combining expression profiles with gene functions, selection constraints, duplication mechanisms, and epigenetic modifications, we unraveled how young duplicate genes were maintained in Arabidopsis genomes

Results

Discussion

Findings

Materials and Methods