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Ancestral polyploidy in seed plants and angiosperms

Abstract

Whole-genome duplication (WGD), or polyploidy, followed by gene loss and diploidization has long been recognized as an important evolutionary force in animals, fungi and other organisms1,2,3, especially plants. The success of angiosperms has been attributed, in part, to innovations associated with gene or whole-genome duplications4,5,6, but evidence for proposed ancient genome duplications pre-dating the divergence of monocots and eudicots remains equivocal in analyses of conserved gene order. Here we use comprehensive phylogenomic analyses of sequenced plant genomes and more than 12.6 million new expressed-sequence-tag sequences from phylogenetically pivotal lineages to elucidate two groups of ancient gene duplications—one in the common ancestor of extant seed plants and the other in the common ancestor of extant angiosperms. Gene duplication events were intensely concentrated around 319 and 192 million years ago, implicating two WGDs in ancestral lineages shortly before the diversification of extant seed plants and extant angiosperms, respectively. Significantly, these ancestral WGDs resulted in the diversification of regulatory genes important to seed and flower development, suggesting that they were involved in major innovations that ultimately contributed to the rise and eventual dominance of seed plants and angiosperms.

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Figure 1: Hypothetical tree topologies and summary of orthogroups consistent with ancient gene duplications before the split of monocots and eudicots.
Figure 2: Age distribution of ancient duplications shared by monocots and eudicots.
Figure 3: Ancestral polyploidy events in seed plants and angiosperms.

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Acknowledgements

This work was supported primarily by NSF Plant Genome Research Program (DEB 0638595, The Ancestral Angiosperm Genome Project) and in part by the Department of Biology and by the Huck Institutes of Life Sciences of the Pennsylvania State University. H.M. was also supported by funds from Fudan University. We thank J. Carlson, M. Frohlich, S. DiLoretto, L. Warg, S. Crutchfield, C. Johnson, N. Naznin, X. Zhou, J. Duarte, B. J. Bliss, J. Der and E. Wafula for help and discussion, D. Stevenson and C. Schultz for Zamia samples, J. McNeal, S. Kim and M. Axtell for photographs, and all the members of The Genome Center at Washington University production team, especially L. Fulton, K. Delehaunty and C. Fronick.

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Authors and Affiliations

Authors

Contributions

Y.J. and C.W.d. designed the study and Y.J. performed the principal data analyses. A.S.C., L.L., P.E.R., Y.H., S.E.S. and H.L. prepared tissues, RNAs, and/or libraries. S.W.C., L.P.T. and S.C.S. generated sequence data. S.A. and J.L.-M. performed the Ancestral Angiosperm Genome Project transcriptome assemblies and MAGIC database construction. Y.J. and C.W.d. drafted the manuscript, and N.J.W., A.S.C., L.L. P.E.R., P.S.S., D.E.S., H.M. and J.L-M. contributed to the planning and discussion of the research and the editing of the manuscript. All authors contributed to and approved the final manuscript.

Corresponding author

Correspondence to Claude W. dePamphilis.

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The authors declare no competing financial interests.

Additional information

Alignments and phylogenetic trees have been deposited in Dryad with package identifier doi:10.5061/dryad.8546.

Supplementary information

Supplementary Information 1

The file contains a Supplementary Discussion, Supplementary References, Supplementary Tables 1-5 and Supplementary Figures 1-8 with legends. (PDF 2117 kb)

Supplementary Table 1

Additional File 1 displays a list of 799 orthogroups with Monocot + Eudicot duplication. (XLS 1635 kb)

Supplementary Table 2

Additional File 2 displays the number of ancient duplications found in orthogroups in all four analyses. (XLS 124 kb)

Supplementary Table 3

Additional File 3 displays data on significant enrichment of GO-SLIM term for the orthogroups with ancient duplication measured by Fisher’s exact test followed by multiple testing corrections. (XLS 27 kb)

Supplementary Information 2

Additional File 4 shows plot of the genomic positions of paralogous pairs of Vitis vinifera genes that arose from duplications prior to the divergence of monocots and eudicots. (PDF 11308 kb)

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Jiao, Y., Wickett, N., Ayyampalayam, S. et al. Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97–100 (2011). https://doi.org/10.1038/nature09916

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