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

Abstract

Whole-genome duplications (WGDs) are widespread and prevalent in vascular plants and frequently coincide with major episodes of global and climatic upheaval, including the mass extinction at the Cretaceous-Tertiary boundary (c. 65 Ma) and during more recent periods of global aridification in the Miocene (c. 10-5 Ma). Here, we explore WGDs in the diverse flowering plant clade Malpighiales. Using transcriptomes and complete genomes from 42 species, we applied a multipronged phylogenomic pipeline to identify, locate, and determine the age of WGDs in Malpighiales using three means of inference: distributions of synonymous substitutions per synonymous site (K_s ) among paralogs, phylogenomic (gene tree) reconciliation, and a likelihood-based gene-count method. We conservatively identify 22 ancient WGDs, widely distributed across Malpighiales subclades. Importantly, these events are clustered around the Eocene-Paleocene transition (c. 54 Ma), during which time the planet was warmer and wetter than any period in the Cenozoic. These results establish that the Eocene Climatic Optimum likely represents a previously unrecognized period of prolific WGDs in plants, and lends further support to the hypothesis that polyploidization promotes adaptation and enhances plant survival during episodes of global change, especially for tropical organisms like Malpighiales, which have tight thermal tolerances.

Keywords: climatic upheaval; flowering plants; genome evolution; global change; phylogenomics; speciation.

Fig. 1

Phylogenetic distribution of whole genome duplications (WGDs) in Malpighiales. Species tree of Malpighiales inferred from 5113 gene trees using a summary coalescent method. WGDs identified from Ks analysis are illustrated with solid black dots on the terminal branches of corresponding species; species indicated with grey dots have transcriptomes that are potentially insufficient for adequate assessment of WGD using the Ks method. Two Salix species are collapsed into one terminal branch for simplicity. Circles illustrated along branches are dated WGDs (divergence time of parental genomes) from our phylogenomic reconciliation analysis. The radius of each circle is proportional to the percentage of orthologus genes supporting the WGD as determined from phylogenomic reconciliation (scale, top left). Solid red circles are significant WGDs as confirmed by our gene-count analysis; solid green circles indicate WGDs that do not receive significant support using the gene count method. Photos on the right are representatives of major Malpighiales clades sampled for investigating whole genome duplications, including from top to bottom (beginning with the left column): Garcinia, Ochna, Tristellateia, Manihot, Viola, Clusia, Linum, Rhizophora, Passiflora, and Salix. Ma, million years ago.

Fig. 2

Age distributions of whole genome duplications (WGDs) among clades of Malpighiales. Density of divergence time of duplicated genes by taxa are plotted in millions of years (Ma). Varying colors refer to different clades exhibiting WGDs (Bhesa excluded for readability). Zachos et al. (2001) curve of global temperature fluctuations during the Cenozoic is redrawn at the top. Mean ages of Gaussian mixture model and variations estimated from bootstrap replicates are indicated by yellow and red bars below the Zachos curve, respectively.