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A genome triplication associated with early diversification of the core eudicots

Yuannian Jiao12, Jim Leebens-Mack3, Saravanaraj Ayyampalayam3, John E Bowers3, Michael R McKain3, Joel McNeal34, Megan Rolf5, Daniel R Ruzicka5, Eric Wafula2, Norman J Wickett26, Xiaolei Wu7, Yong Zhang7, Jun Wang78, Yeting Zhang29, Eric J Carpenter10, Michael K Deyholos10, Toni M Kutchan5, Andre S Chanderbali1112, Pamela S Soltis11, Dennis W Stevenson13, Richard McCombie14, J Chris Pires15, Gane Ka-Shu Wong167, Douglas E Soltis12 and Claude W dePamphilis12*

Author Affiliations

1 Intercollege Graduate Degree Program in Plant Biology, The Pennsylvania State University, University Park, PA 16802, USA

2 Department of Biology, Institute of Molecular Evolutionary Genetics, Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802, USA

3 Department of Plant Biology, University of Georgia, Athens, GA 30602, USA

4 Department of Biology and Physics, Kennesaw State University, Kennesaw, GA 30144, USA

5 Donald Danforth Plant Science Center, 975 North Warson Road, St Louis, MO 63132, USA

6 Division of Plant Science and Conservation, Chicago Botanic Garden, Glencoe, IL 60022, USA

7 Beijing Genomics Institute-Shenzhen, Bei Shan Industrial Zone, Yantian District, Shenzhen 518083, China

8 The Novo Nordisk Foundation Center for Basic Metabolic Research, Department of Biology, University of Copenhagen, Store Kannikestræde 11, 1169 København K, Denmark

9 Intercollege Graduate Degree Program in Genetics, The Pennsylvania State University, University Park, PA 16802, USA

10 Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada

11 Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA

12 Department of Biology, University of Florida, Gainesville, FL 32611, USA

13 New York Botanical Garden, Bronx, New York, NY 10458, USA

14 Genome Research Center, Cold Spring Harbor Laboratory, 500 Sunnyside Blvd, Woodbury, NY 11797, USA

15 Division of Biological Sciences, University of Missouri, Columbia, MI 65211, USA

16 Departments of Biological Sciences and Medicine, Department of Biological Sciences, University of Alberta, Edmonton AB, T6G 2E9, Canada

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Genome Biology 2012, 13:R3  doi:10.1186/gb-2012-13-1-r3

Published: 26 January 2012

Abstract

Background

Although it is agreed that a major polyploidy event, gamma, occurred within the eudicots, the phylogenetic placement of the event remains unclear.

Results

To 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.

Conclusions

The 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.