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Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events

Abstract

Conservation of gene order in vertebrates is evident after hundreds of millions of years of divergence1,2, but comparisons of the Arabidopsis thaliana sequence3 to partial gene orders of other angiosperms (flowering plants) sharing common ancestry 170–235 million years ago4 yield conflicting results5,6,7,8,9,10,11. This difference may be largely due to the propensity of angiosperms to undergo chromosomal duplication (‘polyploidization’) and subsequent gene loss12 (‘diploidization’); these evolutionary mechanisms have profound consequences for comparative biology. Here we integrate a phylogenetic approach (relating chromosomal duplications to the tree of life) with a genomic approach (mitigating information lost to diploidization) to show that a genome-wide duplication3,13,14,15,16,17 post-dates the divergence of Arabidopsis from most dicots. We also show that an inferred ancestral gene order for Arabidopsis reveals more synteny with other dicots (exemplified by cotton), and that additional, more ancient duplication events affect more distant taxonomic comparisons. By using partial sequence data for many diverse taxa to better relate the evolutionary history of completely sequenced genomes to the tree of life, we foster comparative approaches to the study of genome organization, consequences of polyploidy, and the molecular basis of quantitative traits.

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Figure 1: Arrangement of duplicated protein-encoding genes in Arabidopsis thaliana.
Figure 2: Phylogenetic methodology for dating Arabidopsis duplications.
Figure 3: Gene family composition contributes to different levels of divergence between duplicated chromosomal segments.
Figure 4: Examples of Arabidopsis–cotton synteny.

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Acknowledgements

We thank A. Feltus, J. C. Kissinger and S. Schulze for comments on the manuscript, and the Paterson Lab for technical support. This work was supported by the US Department of Agriculture National Research Initiative and Initiative for Future Agriculture and Food Safety, the US National Science Foundation Plant Genome Research Program, the Howard Hughes Medical Institute Graduate Fellowship Program, the International Consortium for Sugarcane Biotechnology, the Georgia Cotton Commission/Cotton Inc., and the Georgia Agricultural Experiment Station.

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Correspondence to Andrew H. Paterson.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Information 1: The unzipped version is an Excel spreadsheet of 9 Mb): this contains the lists of genes and their arrangements in the α,β and γ duplications, and their inferred ancestral gene orders. Note that the file is zipped to save space, and needs to be unzipped to read. (ZIP 2175 kb)

Supplementary Information 2: For each α,β and γ segment pair (labeled in first column), this contains corresponding Arabidopsis chromosomal locations, # genes in the segment pair, frequencies of internal rooted trees for the listed taxa (and in parens, number of trees for each taxon), and likelihood that the number of syntenic duplicated genes between the gene pair would occur by chance based on chi-squared contingency tests calculated reciprocally for the two members of the segment pair (hence two columns). (XLS 1434 kb)

Supplementary Information 3: For each α,β and γ segment pair (labeled in first column), this contains corresponding Arabidopsis chromosomal locations, # genes in the segment pair, frequencies of internal PAM-based pairwise distances for the listed taxa (and in parens, number of trees for each taxon), and likelihood that the number of syntenic duplicated genes between the gene pair would occur by chance based on chi-squared contingency tests calculated reciprocally for the two members of the segment pair (hence two columns). (XLS 67 kb)

Supplementary Information 4: This contains the probe names, 'User_Id’ in GenBank, Genbank accession numbers, chromosomal (homeologous group), map locations, and sequences of the cotton DNA probes used for synteny analysis. (XLS 67 kb)

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Bowers, J., Chapman, B., Rong, J. et al. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422, 433–438 (2003). https://doi.org/10.1038/nature01521

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