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Eukaryotic Cell, September 2006, p. 1517-1531, Vol. 5, No. 9
1535-9778/06/$08.00+0     doi:10.1128/EC.00106-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Evolutionary Origins of the Eukaryotic Shikimate Pathway: Gene Fusions, Horizontal Gene Transfer, and Endosymbiotic Replacements{dagger}

Thomas A. Richards,1,{ddagger} Joel B. Dacks,2 Samantha A. Campbell,3,§ Jeffrey L. Blanchard,4 Peter G. Foster,1 Rima McLeod,5 and Craig W. Roberts3*

Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom,1 Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary T2N 1N4, Canada,2 Department of Immunology, Strathclyde Institute for Biomedical Sciences, University of Strathclyde, 27 Taylor Street, Scotland G4 ONR, United Kingdom,3 Department of Microbiology, University of Massachusetts, Amherst, Massachusetts 01003,4 Departments of Ophthalmology and Visual Sciences, Pediatrics (Infectious Diseases), and Pathology, Committees on Genetics, Molecular Medicine, and Immunology, University of Chicago, Chicago, Illinois 606375

Received 13 April 2006/ Accepted 27 June 2006

Currently the shikimate pathway is reported as a metabolic feature of prokaryotes, ascomycete fungi, apicomplexans, and plants. The plant shikimate pathway enzymes have similarities to prokaryote homologues and are largely active in chloroplasts, suggesting ancestry from the plastid progenitor genome. Toxoplasma gondii, which also possesses an alga-derived plastid organelle, encodes a shikimate pathway with similarities to ascomycete genes, including a five-enzyme pentafunctional arom. These data suggests that the shikimate pathway and the pentafunctional arom either had an ancient origin in the eukaryotes or was conveyed by eukaryote-to-eukaryote horizontal gene transfer (HGT). We expand sampling and analyses of the shikimate pathway genes to include the oomycetes, ciliates, diatoms, basidiomycetes, zygomycetes, and the green and red algae. Sequencing of cDNA from Tetrahymena thermophila confirmed the presence of a pentafused arom, as in fungi and T. gondii. Phylogenies and taxon distribution suggest that the arom gene fusion event may be an ancient eukaryotic innovation. Conversely, the Plantae lineage (represented here by both Viridaeplantae and the red algae) acquired different prokaryotic genes for all seven steps of the shikimate pathway. Two of the phylogenies suggest a derivation of the Plantae genes from the cyanobacterial plastid progenitor genome, but if the full Plantae pathway was originally of cyanobacterial origin, then the five other shikimate pathway genes were obtained from a minimum of two other eubacterial genomes. Thus, the phylogenies demonstrate both separate HGTs and shared derived HGTs within the Plantae clade either by primary HGT transfer or secondarily via the plastid progenitor genome. The shared derived characters support the holophyly of the Plantae lineage and a single ancestral primary plastid endosymbiosis. Our analyses also pinpoints a minimum of 50 gene/domain loss events, demonstrating that loss and replacement events have been an important process in eukaryote genome evolution.

* Corresponding author. Mailing address: Department of Immunology, Strathclyde Institute for Biomedical Sciences, University of Strathclyde, 27 Taylor Street, Scotland G4 ONR, United Kingdom. Phone: 11 141 458 4823. Fax: 11 141 458 48. E-mail: c.w.roberts{at}strath.ac.uk.

{dagger} Supplemental material for this article may be found at http://ec.asm.org/.

{ddagger} Present address: School of Biosciences, University of Exeter, Exeter, EX4 4QD, United Kingdom.

§ Present address: School of Life Sciences, Napier University, 10 Colinton Road, Edinburgh, EH10 5DT, United Kingdom.

Eukaryotic Cell, September 2006, p. 1517-1531, Vol. 5, No. 9
1535-9778/06/$08.00+0     doi:10.1128/EC.00106-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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