Evolution of Gene Duplication in Plants^{<a href="#fn1" rid="fn1" class=" fn">1</a>,}^{<a href="#fn2" rid="fn2" class=" fn">[OPEN]</a>}

Abstract

Distinct from other eukaryotic genomes, plant genomes tend to evolve at higher rates, leading to higher genome diversity (Kejnovsky et al., 2009; Murat et al., 2012). For example, differences in genome size between closely related plant species are much larger than between other closely related eukaryotes. Among dicotyledonous species that diverged approximately 150 million years ago (MYA), genome size ranges from merely 63 Mb in the carnivorous Genlisea margaretae (Greilhuber et al., 2006) to approximately 150 Gb in the canopy plant Paris japonica (Pellicer et al., 2010). This 2,000-fold difference in genome size among dicots is in stark contrast to that observed among the mammalian species that also radiated approximately 150 MYA (Warren et al., 2008), where genome size ranges from approximately 1.6 Gb in Carriker’s round-eared bat (Smith et al., 2013) to approximately 8 Gb in the tetraploid red viscacha rat (Gallardo et al., 1999).

Plant genomes also have an abundance of duplicate genes. Whole-genome duplication (WGD) has occurred multiple times over the past 200 million years of angiosperm evolution (Lyons et al., 2008; Soltis et al., 2009, 2014; Lee et al., 2013; Renny-Byfield and Wendel, 2014), and genomic sequencing continues to reveal new events (Velasco et al., 2010; D’Hont et al., 2012; Wang et al., 2012; Lu et al., 2013; Myburg et al., 2014; Wang et al., 2014b). In contrast, the most recent WGD event occurred approximately 450 MYA in the lineage leading to humans (Panopoulou et al., 2003; Dehal and Boore, 2005) and approximately 200 MYA in the budding yeast lineage (Wolfe and Shields, 1997; Kellis et al., 2004). Strikingly, many plant species also comprise mixed populations of diploid and polyploid individuals, illustrating the prevalence of polyploidy in plants (Husband et al., 2013). For example, 2.4% of Lythrum salicaria populations have both diploid and polyploid individuals (Kubatova et al., 2008), and this percentage is even higher (greater than 60%) for Chamerion angustifolium (Sabara et al., 2013) and Actinidia chinensis (Li et al., 2010).

WGD, or polyploidization, is an extreme mechanism of gene duplication that leads to a sudden increase in both genome size and the entire gene set. However, it is not the only mechanism that gives rise to duplicated genes. In general, gene duplication generates two gene copies; this theoretically allows one or both to evolve under reduced selective constraint and, on some occasions, to acquire novel gene functions that contribute to adaptation. There is little question that duplicate genes have contributed to novel traits over the course of plant evolution (Van de Peer et al., 2009b). Through comparative analyses of an ever-increasing number of plant genome sequences and functional genomic data sets, we now have an unprecedented understanding of how genes are duplicated, how duplicated genes evolve new functions, and the impact of gene duplication on genome evolution (Conant and Wolfe, 2008; Freeling et al., 2015; Soltis et al., 2015).

Gene duplication is but one type of genomic change that can lead to evolutionary novelties. Novel functions can arise from the co-option of existing genes (True and Carroll, 2002), new genes can arise de novo from intergenic space (Tautz and Domazet-Lošo, 2011; Schlötterer, 2015), and new transcriptional regulatory sites can come into existence that alter gene expression (Wray et al., 2003). In addition, although in this review we focus only on genes, the duplication of other genomic features, including regulatory regions (Nourmohammad and Lässig, 2011), transposable elements (TEs; Lisch, 2013), and repeat elements (Sharopova, 2008), has been reported to influence gene expression and function. Nonetheless, gene duplication remains of specific interest both because of the abundance of plant gene duplicates and their potential to contribute to plant novelties. The goal of this review is to provide an overview of our current state of knowledge about plant gene duplication and its significance. We first focus on the prevalence of gene duplication in plants and the mechanisms that contribute to gene duplication. We then discuss the fate of duplicate genes and the factors that influence whether a duplicate is retained or not. Finally, we consider the influence of duplicate genes on the evolution of plant species and agronomically important traits.

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