A genome triplication associated with early diversification of the core eudicots

Yuannian Jiao,Yong Zhang,Xiaolei Wu,Jun Wang,Saravanaraj Ayyampalayam,Eric Wafula,Yeting Zhang,J Chris Pires ,Megan M Rolf ,W Richard Mccombie ,Daniel R Ruzicka ,John E Bowers ,Dennis Wm Stevenson ,Pamela S Soltis ,André S Chanderbali ,Joel R Mcneal ,Toni M Kutchan ,Norman J Wickett ,Michael K Deyholos ,Michael R Mckain ,Eric J Carpenter ,Douglas E Soltis ,Jim Leebens‐Mack ,Gane Ka‐Shu Wong ,Claude W Depamphilis

doi:10.1186/gb-2012-13-1-r3

Abstract

BackgroundAlthough it is agreed that a major polyploidy event, gamma, occurred within the eudicots, the phylogenetic placement of the event remains unclear.ResultsTo determine when this polyploidization occurred relative to speciation events in angiosperm history, we employed a phylogenomic approach to investigate the timing of gene set duplications located on syntenic gamma blocks. We populated 769 putative gene families with large sets of homologs obtained from public transcriptomes of basal angiosperms, magnoliids, asterids, and more than 91.8 gigabases of new next-generation transcriptome sequences of non-grass monocots and basal eudicots. The overwhelming majority (95%) of well-resolved gamma duplications was placed before the separation of rosids and asterids and after the split of monocots and eudicots, providing strong evidence that the gamma polyploidy event occurred early in eudicot evolution. Further, the majority of gene duplications was placed after the divergence of the Ranunculales and core eudicots, indicating that the gamma appears to be restricted to core eudicots. Molecular dating estimates indicate that the duplication events were intensely concentrated around 117 million years ago.ConclusionsThe rapid radiation of core eudicot lineages that gave rise to nearly 75% of angiosperm species appears to have occurred coincidentally or shortly following the gamma triplication event. Reconciliation of gene trees with a species phylogeny can elucidate the timing of major events in genome evolution, even when genome sequences are only available for a subset of species represented in the gene trees. Comprehensive transcriptome datasets are valuable complements to genome sequences for high-resolution phylogenomic analysis.

Highlights

It is agreed that a major polyploidy event, gamma, occurred within the eudicots, the phylogenetic placement of the event remains unclear
Since the g event was first identified in a groundbreaking phylogenomic analysis of the Arabidopsis genome [9], its timing has been hypothesized to have predated the origin of angiosperms, the divergence of monocots and eudicots and the divergence of asterid and rosid eudicot clades (Figure 1)
Most recent analyses suggest that g occurred within the eudicots, but the timing of the g event relative to the diversification of core eudicots remains unclear [13]

Summary

Introduction

It is agreed that a major polyploidy event, gamma, occurred within the eudicots, the phylogenetic placement of the event remains unclear. Synteny-based and phylogenomic analyses of the Arabidopsis genome revealed multiple WGD events [8,9] The oldest of these WGD events was placed before the monocot-eudicot divergence, a second WGD was hypothesized to be shared among most, if not all, eudicots, and a more recent WGD was inferred to have occurred before diversification of the Brassicales [9]. Comparisons of available genome sequences for other core rosid species (including Carica, Populus, and Arabidopsis) and the recently sequenced potato genome (an asterid, Solanum tuberosum) show evidence of one or more rounds of polyploidy with the most ancient event within each genome represented by triplicated gene blocks showing interspecific synteny with triplicated blocks in the Vitis genome [7,11,34,35]. The most parsimonious explanation of these patterns is that g occurred in a common ancestor of rosids and asterids, because all sequenced genomes within these lineages share a triplicate genome structure [12,35]

Methods

Results

Conclusion