Modes of Gene Duplication Contribute Differently to Genetic Novelty and Redundancy, but Show Parallels across Divergent Angiosperms

Yupeng Wang,F Alex Feltus,Andrew H Paterson,Xiyin Wang,Xu Tan,Stephen P Ficklin,Haibao Tang,Stephen R Proulx

doi:10.1371/journal.pone.0028150

Abstract

BackgroundBoth single gene and whole genome duplications (WGD) have recurred in angiosperm evolution. However, the evolutionary effects of different modes of gene duplication, especially regarding their contributions to genetic novelty or redundancy, have been inadequately explored.ResultsIn Arabidopsis thaliana and Oryza sativa (rice), species that deeply sample botanical diversity and for which expression data are available from a wide range of tissues and physiological conditions, we have compared expression divergence between genes duplicated by six different mechanisms (WGD, tandem, proximal, DNA based transposed, retrotransposed and dispersed), and between positional orthologs. Both neo-functionalization and genetic redundancy appear to contribute to retention of duplicate genes. Genes resulting from WGD and tandem duplications diverge slowest in both coding sequences and gene expression, and contribute most to genetic redundancy, while other duplication modes contribute more to evolutionary novelty. WGD duplicates may more frequently be retained due to dosage amplification, while inferred transposon mediated gene duplications tend to reduce gene expression levels. The extent of expression divergence between duplicates is discernibly related to duplication modes, different WGD events, amino acid divergence, and putatively neutral divergence (time), but the contribution of each factor is heterogeneous among duplication modes. Gene loss may retard inter-species expression divergence. Members of different gene families may have non-random patterns of origin that are similar in Arabidopsis and rice, suggesting the action of pan-taxon principles of molecular evolution.ConclusionGene duplication modes differ in contribution to genetic novelty and redundancy, but show some parallels in taxa separated by hundreds of millions of years of evolution.

Highlights

Genes may be duplicated by several mechanisms in addition to whole genome duplications (WGD), which have been collectively referred to as small scale duplications [34] or single gene duplications [35,36]
We classified gene duplications into six modes: WGD, tandem, proximal, DNA based transposed, retrotransposed and dispersed duplication, according to the procedure shown in Figure 1 and described in methods
We propose that WGD events themselves, together with the subsequent ‘adaptation’ of the resulting genome to the newly-duplicated state, may accelerate evolution, contributing to variation in expression divergence sometimes attributed to time alone [58,60]

Summary

Introduction

Whole-genome duplications (WGDs) have occurred in the lineages of plants [1], animals [2,3] and fungi [4,5], with possible consequences including evolution of novel or modified gene functions [6,7,8,9], and/or provision of ‘‘buffer capacity’’ [10,11] or genetic redundancy that increases genetic robustness [12,13,14,15,16,17]. Tandem duplicates are consecutive in the genome while proximal duplicates are near one another but separated by a few genes These two gene duplication modes are presumed to arise through unequal crossing over [36] or localized transposon activities [37]. The new retrogene is often deposited in a novel chromosomal environment with new (i.e. nonancestral) neighboring genes and, having lost its native promoter, is only likely to survive as a functional gene if a new promoter is acquired [41,42]. Both single gene and whole genome duplications (WGD) have recurred in angiosperm evolution. The evolutionary effects of different modes of gene duplication, especially regarding their contributions to genetic novelty or redundancy, have been inadequately explored

Methods

Results

Discussion

Conclusion