Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns

  1. Robert K. Jansen,,
  2. Zhengqiu Cai,
  3. Linda A. Raubeson§,
  4. Henry Daniell,
  5. Claude W. dePamphilis,
  6. James Leebens-Mack††,
  7. Kai F. Müller,‡‡,
  8. Mary Guisinger-Bellian,
  9. Rosemarie C. Haberle,
  10. Anne K. Hansen,
  11. Timothy W. Chumley,
  12. Seung-Bum Lee,
  13. Rhiannon Peery§,
  14. Joel R. McNeal††,
  15. Jennifer V. Kuehl§§, and
  16. Jeffrey L. Boore§§,¶¶
  1. Section of Integrative Biology and Institute of Cellular and Molecular Biology, University of Texas, Austin, TX 78712;
  2. §Department of Biological Sciences, Central Washington University, Ellensburg, WA 98926;
  3. Department of Molecular Biology and Microbiology, Biomolecular Science, University of Central Florida, Orlando, FL 32816;
  4. Department of Biology and Institute of Molecular and Evolutionary Genetics, Huck Institutes of Life Sciences, Pennsylvania State University, University Park, PA 16802;
  5. ††Department of Plant Biology, University of Georgia, Athens, GA 30602;
  6. §§Department of Energy Joint Genome Institute and Lawrence Berkeley National Laboratory, Walnut Creek, CA 94598; and
  7. ‡‡Nees Institute for Biodiversity of Plants, University of Bonn, 53115 Bonn, Germany
  1. Communicated by Peter H. Raven, Missouri Botanical Garden, St. Louis, MO, September 25, 2007 (received for review July 6, 2007)

Abstract

Angiosperms are the largest and most successful clade of land plants with >250,000 species distributed in nearly every terrestrial habitat. Many phylogenetic studies have been based on DNA sequences of one to several genes, but, despite decades of intensive efforts, relationships among early diverging lineages and several of the major clades remain either incompletely resolved or weakly supported. We performed phylogenetic analyses of 81 plastid genes in 64 sequenced genomes, including 13 new genomes, to estimate relationships among the major angiosperm clades, and the resulting trees are used to examine the evolution of gene and intron content. Phylogenetic trees from multiple methods, including model-based approaches, provide strong support for the position of Amborella as the earliest diverging lineage of flowering plants, followed by Nymphaeales and Austrobaileyales. The plastid genome trees also provide strong support for a sister relationship between eudicots and monocots, and this group is sister to a clade that includes Chloranthales and magnoliids. Resolution of relationships among the major clades of angiosperms provides the necessary framework for addressing numerous evolutionary questions regarding the rapid diversification of angiosperms. Gene and intron content are highly conserved among the early diverging angiosperms and basal eudicots, but 62 independent gene and intron losses are limited to the more derived monocot and eudicot clades. Moreover, a lineage-specific correlation was detected between rates of nucleotide substitutions, indels, and genomic rearrangements.

Footnotes

  • To whom correspondence should be addressed. E-mail: jansen{at}mail.utexas.edu
  • Author contributions: R.K.J. designed research; Z.C., L.A.R., H.D., C.W.d., J.L.-M., M.G.-B., R.C.H., A.K.H., T.W.C., S.-B.L., R.P., J.R.M., J.V.K., and J.L.B. performed research; R.K.J., Z.C., L.A.R., J.L.-M., and K.F.M. analyzed data; and R.K.J. wrote the paper.

  • ¶¶Present addresses: Genome Project Solutions, 1024 Promenade Street, Hercules, CA 94547; and University of California, 3060 VLSB, Berkeley, CA 94702.

  • The authors declare no conflict of interest.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession numbers are provided in SI Table 1). The aligned data matrix is available at http://chloroplast.cbio.psu.edu.

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0709121104/DC1.

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