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MBE Advance Access published online on June 3, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn129
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© The Author 2008. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

Frequent, phylogenetically local horizontal transfer of the cox1 group I intron in flowering plant mitochondria

M. Virginia Sanchez-Puerta1,*, Yangrae Cho1,2, Jeffrey P. Mower1,3, Andrew J. Alverson1 and Jeffrey D. Palmer1

1 Department of Biology, Indiana University, Bloomington, IN 47405, USA
2 Department of Plant & Environmental Protection Sciences, University of Hawaii-Manoa, Honolulu, HI 96822, USA
3 Smurfit Institute of Genetics, Trinity College Dublin, Dublin 2, Ireland

* Corresponding author: M. Virginia Sanchez-Puerta, 1001 East 3rd St, Indiana University, Bloomington, IN 47405, USA; Tel: 1 812 855 2549; Fax: 1 812 855 6705; Email: mvs{at}indiana.edu

Received for publication January 24, 2008. Revision received May 9, 2008. Revision received May 27, 2008. Accepted for publication May 27, 2008.

Horizontal gene transfer is surprisingly common among plant mitochondrial genomes. The first well-established case involves a homing group I intron in the mitochondrial cox1 gene shown to have been frequently acquired via horizontal transfer in angiosperms. Here we report extensive additional sampling of angiosperms, including 85 newly sequenced introns from 30 families. Analysis of all available data leads us to conclude that, among the 640 angiosperms (from 212 families) whose cox1 intron status has been characterized thus far, the intron has been acquired via roughly 70 separate horizontal transfer events. We propose that the intron was originally seeded into angiosperms by a single transfer from fungi, with all subsequent inferred transfers occurring from one angiosperm to another. The pattern of angiosperm-to-angiosperm transfer is biased towards exchanges between plants belonging to the same family. Illegitimate pollination is proposed as one potential factor responsible for this pattern, given that aberrant, cross-species pollination is more likely between close relatives. Other potential factors include shared vectoring agents or common geographic locations. We report the first apparent cases of loss of the cox1 intron; losses are accompanied by retention of the exonic coconversion tract, which is located immediately downstream of the intron and which is a product of the intron's self-insertion mechanism. We discuss the many reasons why the cox1 intron is so frequently and detectably transferred, and rarely lost, and conclude that it should be regarded as the "canary in the coal mine" with respect to horizontal transfer in angiosperm mitochondria.

Key Words: cox1 • group I intron • horizontal transfer • angiosperm • homing endonuclease


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