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      A genome triplication associated with early diversification of the core eudicots

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          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.

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          Most cited references38

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          The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla.

          The analysis of the first plant genomes provided unexpected evidence for genome duplication events in species that had previously been considered as true diploids on the basis of their genetics. These polyploidization events may have had important consequences in plant evolution, in particular for species radiation and adaptation and for the modulation of functional capacities. Here we report a high-quality draft of the genome sequence of grapevine (Vitis vinifera) obtained from a highly homozygous genotype. The draft sequence of the grapevine genome is the fourth one produced so far for flowering plants, the second for a woody species and the first for a fruit crop (cultivated for both fruit and beverage). Grapevine was selected because of its important place in the cultural heritage of humanity beginning during the Neolithic period. Several large expansions of gene families with roles in aromatic features are observed. The grapevine genome has not undergone recent genome duplication, thus enabling the discovery of ancestral traits and features of the genetic organization of flowering plants. This analysis reveals the contribution of three ancestral genomes to the grapevine haploid content. This ancestral arrangement is common to many dicotyledonous plants but is absent from the genome of rice, which is a monocotyledon. Furthermore, we explain the chronology of previously described whole-genome duplication events in the evolution of flowering plants.
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            Synteny and collinearity in plant genomes.

            Correlated gene arrangements among taxa provide a valuable framework for inference of shared ancestry of genes and for the utilization of findings from model organisms to study less-well-understood systems. In angiosperms, comparisons of gene arrangements are complicated by recurring polyploidy and extensive genome rearrangement. New genome sequences and improved analytical approaches are clarifying angiosperm evolution and revealing patterns of differential gene loss after genome duplication and differential gene retention associated with evolution of some morphological complexity. Because of variability in DNA substitution rates among taxa and genes, deviation from collinearity might be a more reliable phylogenetic character.
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              Polyploidy and genome evolution in plants.

              Genome doubling (polyploidy) has been and continues to be a pervasive force in plant evolution. Modern plant genomes harbor evidence of multiple rounds of past polyploidization events, often followed by massive silencing and elimination of duplicated genes. Recent studies have refined our inferences of the number and timing of polyploidy events and the impact of these events on genome structure. Many polyploids experience extensive and rapid genomic alterations, some arising with the onset of polyploidy. Survivorship of duplicated genes are differential across gene classes, with some duplicate genes more prone to retention than others. Recent theory is now supported by evidence showing that genes that are retained in duplicate typically diversify in function or undergo subfunctionalization. Polyploidy has extensive effects on gene expression, with gene silencing accompanying polyploid formation and continuing over evolutionary time.
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                Author and article information

                Journal
                Genome Biol
                Genome Biol
                Genome Biology
                BioMed Central
                1465-6906
                1465-6914
                2012
                26 January 2012
                : 13
                : 1
                : R3
                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
                Article
                gb-2012-13-1-r3
                10.1186/gb-2012-13-1-r3
                3334584
                22280555
                84eda653-1029-44bf-8f76-0e37b78a633f
                Copyright ©2012 Jiao et al.; licensee BioMed Central Ltd.

                This is an open access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 3 November 2011
                : 26 January 2012
                Categories
                Research

                Genetics
                Genetics

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