Abstract

Polyploidy has contributed to the divergence and domestication of plants; however, estimation of the relative roles that different types of polyploidy have played during evolution has been difficult. Unbalanced and balanced gene removal was previously related to allopolyploidies and autopolyploidies, respectively. Here, to infer the types of polyploidies and evaluate their evolutionary effects, we devised a statistic, the Polyploidy-index or P-index, to characterize the degree of divergence between subgenomes of a polyploidy, to find whether there has been a balanced or unbalanced gene removal from the homoeologous regions. Based on a P-index threshold of 0.3 that distinguishes between known or previously inferred allo- or autopolyploidies, we found that 87.5% of 24 angiosperm paleo-polyploidies were likely produced by allopolyploidizations, responsible for establishment of major tribes such as Poaceae and Fabaceae, and large groups such as monocots and eudicots. These findings suggest that >99.7% of plant genomes likely derived directly from allopolyploidies, with autopolyploidies responsible for the establishment of only a few small genera, including Glycine, Malus, and Populus, each containing tens of species. Overall, these findings show that polyploids with high divergence between subgenomes (presumably allopolyploids) established the major plant groups, possibly through secondary contact between previously isolated populations and hybrid vigor associated with their re-joining.

Highlights

  • Polyploidy is a state in which an organism or cell contains two or more basic sets of chromosomes (Van de Peer et al, 2017)

  • When calculating P-index, a reference genome was used to show orthologous gene colinearity with the studied genome, and checking the intervening non-collinear genes would show likely gene losses in each of the inferred subgenomes produced by a paleopolyploidization event

  • We explored gene losses in 44 well-assembled angiosperm genomes affected by polyploidies (Figure 1) and characterized their P-indices during the evolution of these species (Figure 2)

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Summary

Introduction

Polyploidy is a state in which an organism or cell contains two or more basic sets of chromosomes (Van de Peer et al, 2017). An autopolyploid is formed by duplicating a genome, whereas an allopolyploid is derived from hybridization between different species with some independent evolutionary history, followed by chromosome doubling or fusion of unreduced gametes. The prevalence of different types of plant polyploidies has long been a topic of debate (Barker et al, 2016; Soltis et al, 2016). Autopolyploids are thought to form more frequently and involve fewer incompatibilities between the merged genomes, but allopolyploids may offer greater advantages to a new lineage due to their potential for permanent intergenomic heterosis (Ramsey and Schemske, 2002). A recent survey indicated that across 47 vascular plant genera, 13% and 11% of plant species could be inferred as auto- and allopolyploids, respectively (Barker et al, 2016)

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