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Widespread horizontal transfer of mitochondrial genes in flowering plants

Nature volume 424, pages 197–201 (2003)Cite this article

Abstract

Horizontal gene transfer—the exchange of genes across mating barriers—is recognized as a major force in bacterial evolution1,2. However, in eukaryotes it is prevalent only in certain phagotrophic protists and limited largely to the ancient acquisition of bacterial genes3,4,5. Although the human genome was initially reported6 to contain over 100 genes acquired during vertebrate evolution from bacteria, this claim was immediately and repeatedly rebutted7,8. Moreover, horizontal transfer is unknown within the evolution of animals, plants and fungi except in the special context of mobile genetic elements9,10,11,12. Here we show, however, that standard mitochondrial genes, encoding ribosomal and respiratory proteins, are subject to evolutionarily frequent horizontal transfer between distantly related flowering plants. These transfers have created a variety of genomic outcomes, including gene duplication, recapture of genes lost through transfer to the nucleus, and chimaeric, half-monocot, half-dicot genes. These results imply the existence of mechanisms for the delivery of DNA between unrelated plants, indicate that horizontal transfer is also a force in plant nuclear genomes, and are discussed in the contexts of plant molecular phylogeny and genetically modified plants.

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Figure 1: Anomalous presence of ribosomal protein genes in three angiosperm mitochondrial DNAs. A consensus phylogeny of 280 angiosperms is marked according to the presence (red branches) or absence (blue branches) of rps2 (a) and rps11 (b) in mitochondrial DNA (tree topology and gene presence/absence data are from ref.
Figure 2: Phylogenetic evidence for HGT in angiosperm mitochondrial DNA.
Figure 3: Chimaeric structure of the Sanguinaria rps11 gene.
Figure 4: Approximate timing and donor–recipient relationships of five HGT ‘events’ in angiosperm mitochondrial DNA.

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Acknowledgements

We thank C. Mathews for technical assistance; E. Knox for creating Fig. 4, for drafting Fig. 1 and for discussion; L. Goertzen, E. Knox, R. Olmstead, D. Rice and S. Stefanovic for critical reading of the manuscript; R. Gardner for providing several Actinidia DNAs; M. Stoutemyer and J. Gastony for help in obtaining plant material; and B. Hall and the University of California Santa Cruz arboretum for supplying leaf material for Amborella. Financial support was provided by the US NIH.

Author information

Authors and Affiliations

  1. Department of Biology, Indiana University, Bloomington, Indiana, 47405, USA

    Ulfar Bergthorsson, Keith L. Adams, Brendan Thomason & Jeffrey D. Palmer

  2. Department of Botany, Iowa State University, Iowa, Ames, 50011, USA

    Keith L. Adams

  3. Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan, 48109, USA

    Brendan Thomason

Authors
  1. Ulfar Bergthorsson
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  2. Keith L. Adams
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  4. Jeffrey D. Palmer
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Correspondence to Jeffrey D. Palmer.

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Supplementary information

41586_2003_BFnature01743_MOESM1_ESM.pdf

Supplementary Figure 1: Phylogenetic trees of rps2 and rps11 that show much greater divergence of nuclear than mitochondrial genes in plants. (PDF 192 kb)

Supplementary Figure 2: Nucleotide alignment used for the rps2 analysis shown in Fig. 2a of the main text. (PDF 84 kb)

41586_2003_BFnature01743_MOESM3_ESM.pdf

Supplementary Figure 3: Nucleotide alignment used for the rps11 analysis shown in Fig. 2b, 2d and 2e of the main text. (PDF 134 kb)

Supplementary Figure 4: Nucleotide alignment used for the atp1 analysis shown in Fig. 2f of the main text. (PDF 378 kb)

41586_2003_BFnature01743_MOESM5_ESM.pdf

Supplementary Figure 5: Nucleotide alignment used for the rps11 upstream sequence analysis shown in Fig. 2c of the main text. (PDF 36 kb)

Supplementary Figure Legends (DOC 21 kb)

Supplementary Table 1: Primers for PCR and DNA sequencing used in this study. (DOC 30 kb)

41586_2003_BFnature01743_MOESM8_ESM.doc

Supplementary Information: 1) Ruling out DNA contamination or mix-up, 2) Mitochondrial provenance of horizontally-acquired plant genes, 3) The tip of an iceberg of mitochondrial HGT in plants, 4) Parametric bootstrapping 5) Supplemental references. (DOC 50 kb)

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Bergthorsson, U., Adams, K., Thomason, B. et al. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424, 197–201 (2003). https://doi.org/10.1038/nature01743

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