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MBE Advance Access originally published online on May 4, 2006
Molecular Biology and Evolution 2006 23(7):1437-1443; doi:10.1093/molbev/msl008
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© The Author 2006. 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

Lateral Gene Transfer of a Multigene Region from Cyanobacteria to Dinoflagellates Resulting in a Novel Plastid-Targeted Fusion Protein

Ross F. Waller1, Claudio H. Slamovits and Patrick J. Keeling

Canadian Institute for Advanced Research, Botany Department, University of British Columbia, Vancouver, British Columbia, Canada

E-mail: r.waller{at}unimelb.edu.au.

The number of cases of lateral or horizontal gene transfer in eukaryotic genomes is growing steadily, but in most cases, neither the donor nor the recipient is known, and the biological implications of the transfer are not clear. We describe a relatively well-defined case of transfer from a cyanobacterial source to an ancestor of dinoflagellates that diverged before Oxyrrhis but after Perkinsus. This case is also exceptional in that 2 adjacent genes, a paralogue of the shikimate biosynthetic enzyme AroB and an O-methyltransferase (OMT) were transferred together and formed a fusion protein that was subsequently targeted to the dinoflagellate plastid. Moreover, this fusion subsequently reverted to 2 individual genes in the genus Karlodinium, but both proteins maintained plastid localization with the OMT moiety acquiring its own plastid-targeting peptide. The presence of shikimate biosynthetic enzymes in the plastid is not unprecedented as this is a plastid-based pathway in many eukaryotes, but this species of OMT has not been associated with the plastid previously. It appears that the OMT activity was drawn into the plastid simply by virtue of its attachment to the AroB paralogue resulting from their cotransfer and once in the plastid performed some essential function so that it remained plastid targeted after it separated from AroB. Gene fusion events are considered rare and likely stable, and such an event has recently been used to argue for a root of the eukaryotic tree. Our data, however, show that exact reversals of fusion events do take place, and hence gene fusion data are difficult to interpret without knowledge of the phylogeny of the organisms—therefore their use as phylogenetic markers must be considered carefully.

Key Words: lateral gene transfer • dinoflagellates • gene fusion • gene fission


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