Is post-polyploidization diploidization the key to the evolutionary success of angiosperms?

Abstract

Advances in recent years have revolutionized our understanding of both the context and occurrence of polyploidy in plants. Molecular phylogenetics has vastly improved our understanding of plant relationships, enabling us to better understand trait and character evolution, including chromosome number changes. This, in turn, has allowed us to appreciate better the frequent occurrence and extent of polyploidy throughout the history of angiosperms, despite the occurrence of low chromosome numbers in some groups, such as in Arabidopsis (A. thaliana was the first plant genome to be sequenced and assembled). In tandem with an enhanced appreciation of phylogenetic relationships, the accumulation of genomic data has led to the conclusion that all angiosperms are palaeopolyploids, together with better estimates of the frequency and type of polyploidy in different angiosperm lineages. The focus therefore becomes when a lineage last underwent polyploidization, rather than simply whether a plant is ‘diploid’ or ‘polyploid’. This legacy of past polyploidization in plants is masked by large‐scale genome reorganization involving repetitive DNA loss, chromosome rearrangements (including fusions and fissions) and complex patterns of gene loss, a set of processes that are collectively termed ‘diploidization’. We argue here that it is the diploidization process that is responsible for the ‘lag phase’ between polyploidization events and lineage diversification. If so, diploidization is important in determining chromosome structure and gene content, and has therefore made a significant contribution to the evolutionary success of flowering plants. © 2015 The Authors. Botanical Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of Linnean Society of London, 2016, 180, 1–5.

Time-calibrated phylogenetic trees establish a lag between polyploidisation and diversification in Nicotiana (Solanaceae)

“…Increases in net diversification rates tend to follow a lag phase post-polyploidisation, adding support to the previously proposed model (Schranz et al 2012;Tank et al 2015). It therefore seems probable that at the genomic level the progression of events associated with diploidisation is an important factor in understanding the lag phase (Dodsworth et al 2016a).…”

“…Some allopolyploids are recent and have no close polyploid relatives, whereas others appear to be much older and numerous, the result of speciation at the polyploid level. Polyploidy and diploidisation have been the subject of study in the genus for around two decades: chromosome arm translocations (Lim et al 2004), homoploid hybridisation , intergenic recombination , concerted evolution , long-term diploidisation of genomic repeats (Clarkson et al 2005;Dodsworth et al 2016a), progenitor determination (Kelly et al 2013), maternal genome donors , elimination of genomic repeats (Renny-Byfield et al 2011), the phylogenetic signal in repeats (Dodsworth et al 2015(Dodsworth et al , 2016b, floral evolution (McCarthy et al 2015), morphological character evolution (Marks et al 2011a;McCarthy et al 2016), biogeography (Ladiges et al 2011) and genome size changes (Leitch et al 2008). An earlier paper (Clarkson et al 2005) focused on the timing of polyploid events for a subset of polyploids in Nicotiana, using nonparametric rate smoothing (NPRS), but recent advances in molecular clock analysis make another study of this subject in the genus as a whole timely.…”

“…Astonishing levels of duplication have been documented in some angiosperms; for example, it has been estimated that Gossypium has a ploidy level of 144x (Wendel 2015). Each round of polyploidy is followed by diploidisation [see Dodsworth et al (2016a)], which involves gene loss (often preferentially from one progenitor, i.e. biased fractionation), chromosome reorganisation, chromosome fusion and overall genome size reduction (Wendel 2015).…”

The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications

“…These reports strengthen the WGD Radiation Lag-Time Model formalized by Schranz et al (2012), who found that in six examples of angiosperm radiations a species-poor sister-group shared a WGD event with the species-rich crown group, directly contradicting the notion that WGD was the sole immediate cause of these radiations. The lag between WGD and subsequent radiations thus has been proposed as evidence that the long and stochastic process of polyploid drop is the proximal engine of speciation and cladogenesis (Dodsworth et al, 2016;Clark and Donoghue, 2017;Mandáková and Lysak, 2018).…”

Evolution of floral diversity: genomics, genes andgamma

“…polyploidy) in the origin and subsequent diversification of flowering plants [31][32][33][34][35][36][37]. For example, an ancient polyploidy event has been inferred for the common ancestor of all angiosperms [38,39], three sequential polyploidy events in the monocots pre-date the radiation of the grasses [40,41] and ancient hexaploidy characterizes most eudicots [42][43][44][45].…”