Polyploid Evolution of the Brassicaceae during the Cenozoic Era    

Abstract

The Brassicaceae (Cruciferae) family, owing to its remarkable species, genetic, and physiological diversity as well as its significant economic potential, has become a model for polyploidy and evolutionary studies. Utilizing extensive transcriptome pyrosequencing of diverse taxa, we established a resolved phylogeny of a subset of crucifer species. We elucidated the frequency, age, and phylogenetic position of polyploidy and lineage separation events that have marked the evolutionary history of the Brassicaceae. Besides the well-known ancient a (47 million years ago [Mya]) and b (124 Mya) paleopolyploidy events, several species were shown to have undergone a further more recent (;7 to 12 Mya) round of genome multiplication. We identified eight whole-genome duplications corresponding to at least five independent neo/mesopolyploidy events. Although the Brassicaceae family evolved from other eudicots at the beginning of the Cenozoic era of the Earth (60 Mya), major diversification occurred only during the Neogene period (0 to 23 Mya). Remarkably, the widespread species divergence, major polyploidy, and lineage separation events during Brassicaceae evolution are clustered in time around epoch transitions characterized by prolonged unstable climatic conditions. The synchronized diversification of Brassicaceae species suggests that polyploid events may have conferred higher adaptability and increased tolerance toward the drastically changing global environment, thus facilitating species radiation.

A Time-Calibrated Road Map of Brassicaceae Species Radiation and Evolutionary History

“…Fossil constraints and tree root height are indicated accordingly. The a-WGD was placed on the figure at 47 million years (maximum age estimated in Kagale et al, 2014). Divergence times are indicated with 95% confidence intervals.…”

“…However, in an angiosperm-wide time-calibrated phylogeny including all reliable fossils, the Caricaceae node was set to 81.6 million years (Magallón et al, 2015), thereby corresponding to the maximum age of the b-WGD. The discrepancy might be explained by the different approaches used to calculate divergence times: via relaxed evolutionary models (Magallón et al, 2015) or extrapolating a constant synonymous substitution rate (Kagale et al, 2014). Recently, a Brassicales-wide transcriptome analysis provided phylogenetic placements of these two genome duplication events and the estimates are 40 and 88 mya for At-a and At-b, respectively (Edger et al, 2015).…”

“…This WGD was first shown by Vision et al (2000) and Bowers et al (2003), later shown to be Brassicaceaespecific (Schranz et al, 2012;Haudry et al, 2013;Hofberger et al, 2013), and recently its maximum age was estimated to 47.1 million years ago (mya; Kagale et al, 2014), thereby also providing the maximum age of the Brassicaceae stem group. The older b-WGD (At-b) was dated to 124 mya (Kagale et al, 2014) and is assumed not to be shared with the Caricaceae (Ming et al, 2008). However, in an angiosperm-wide time-calibrated phylogeny including all reliable fossils, the Caricaceae node was set to 81.6 million years (Magallón et al, 2015), thereby corresponding to the maximum age of the b-WGD.…”

“…However, the total number of mesopolyploidization events might be higher, considering isolated lineages characterized by extreme long branches in molecular phylogenetic reconstructions, as exemplified by the tribes Kernereae, Buniadeae, Heliophileae, and Cochlearieae. Some additional mesopolyploidy events have been postulated (Pringlea and Stanleya [Kagale et al, 2014] and Caulanthus [Burrell et al, 2011], all from tribe Thelypodieae; Physarieae [Lysak et al, 2009]), pending further validation.…”

“…Some of this diversification is correlated with polyploidization. Because WGDs are assumed to have played a major role in the speciation and diversification of angiosperms (De Bodt et al, 2005;Soltis et al, 2009;Tang et al, 2010;Jiao et al, 2011), the significance of ancient polyploidy has also been investigated across the Brassicaceae family (Lysak et al, 2009;Franzke et al, 2011;Lysak and Koch, 2011;Kagale et al, 2014). Based on the elapsed time since their occurrence and the level of genome diploidization, WGDs have been classified into three categories, as neo-, meso-, and paleopolyploid events (Mandáková et al, 2010a;Lysak and Koch, 2011;Kagale et al, 2014).…”