Widespread ancient whole genome duplications in Malpighiales coincide with Eocene global climatic upheaval

Abstract

. CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/215608 doi: bioRxiv preprint first posted online Nov. 7, 2017; Cai et al. 4 Whole genome duplication (WGD), or polyploidy, is an important evolutionary force that has shaped plant evolution. It has long been appreciated that the formation of recent polyploids in vascular plants is common (1, 2), and mounting evidence suggests that ancient polyploids are more frequent than once thought.Well-cited examples of ancient WGDs have been associated with the origin of several hyperdiverse clades, including in the common ancestor of seed plants, flowering plants, monocots, orchids, core eudicots, mustards (Brassicaceae), legumes (Fabaceae), and sunflowers (Asteraceae) (3-13). In addition, WGDs have been identified in ferns and gymnosperms (14, 15), thus expanding the phylogenetic scope of this phenomenon to span vascular plants. Among these ancient WGDs, several have been dated to the Cretaceous-Tertiary (KT) boundary (~65 Ma), potentially linking these polyploidization events to plants' abilities to survive abrupt global environmental change (16, 17). Similarly, a large number of WGDs have also been reported in grasses during the late Miocene when arid, grass dominated landscapes expanded dramatically (18). In these cases, the potential adaptive value of WGDs is thought to arise from the origin of genetic novelties (19)(20)(21)(22) and by masking the effects of deleterious mutations (23), which may facilitate plant survival across periods of global disruption. Although debate exists as to the influence of WGD on speciation and enhanced species diversification rates (14,(24)(25)(26)(27)(28), it is generally accepted that chromosomal rearrangements from WGDs can significantly accelerate isolating barriers, thus promoting cladogenesis (29-31). In short, it is established that WGDs are a prominent feature of vascular plant evolution, but the respective phylogenetic distribution, timing, and significance of these ancient events remains unclear.Here, we investigate WGDs in the large and diverse angiosperm order Malpighiales, which contains more than 16,000, mostly tropical, species with tremendous morphological and ecological diversity. Members of this clade also include numerous economically important crops such as rubber, cassava, and flax. The Malpighiales have long been recognized as one of the most difficult clades to resolve in the flowering plant tree of life (32, 33), which has been attributed in part to its rapid radiation in the mid-Cretaceous (33, 34). However, recent efforts utilizing phylogenomic approaches have greatly increased our . CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/215608 doi: bioRxiv preprint first posted online Nov. 7, 2017; Cai et al. 5understanding of deep level rel...

Polyploidy as a mechanism for surviving global change

“…In summary, the results presented by Cai et al . have implications for numerous areas of interest in the ever‐growing field of plant polyploidy research.…”

“…While not all major bursts of diversification in plant evolution are associated with polyploidy, the correlation is too strong to ignore the legacy of WGD in shaping plant diversity through time. While Cai et al . did not test directly for a relationship between WGD and changes in net diversification rate across Malpighiales, they do note that overall there appears to be a strong association of WGD with the most diverse clades in the order.…”

“…Much of the work on plant polyploidy has focused necessarily on extant taxa, but phylogenetic approaches have allowed researchers to identify WGDs that occurred putatively many millions of years ago, including in the ancestry of all major land plant and algal lineages examined to date ( One Thousand Plant Transcriptomes Initiative , unpublished). In this issue of New Phytologist , Cai et al . (pp. 565–576) extend these insights into the past one step further and identify not only a remarkable number of WGD events in the history of the plant order Malpighiales, but a significant correlation between the timing of these events and periods of global climatic change during the Paleocene–Eocene transition and in the late Miocene, c .…”

“…Cai et al . employed a suite of methods to identify and date the occurrence of WGD events across the Malpighiales.…”

“…The relationship between WGD and the success of lineages during periods of global change is a particularly compelling avenue that deserves further attention across the plant tree of life. This study on Malpighiales and the multi‐pronged approach that Cai et al . used to identify and date WGD events should serve as a gold standard for other researchers wishing to use genomic and transcriptomic tools to study paleopolyploidy in their clades of interest.…”