Evolutionary origins of the eukaryotic shikimate pathway: gene fusions, horizontal gene transfer, and endosymbiotic replacements

Thomas A Richards, Joel B Dacks, Samantha A Campbell, Jeffrey L Blanchard, Peter G Foster, Rima McLeod, Craig W Roberts

Research output: Contribution to journalArticle

116 Citations (Scopus)

Abstract

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.
LanguageEnglish
Pages1517-1531
Number of pages15
JournalEukaryotic Cell
Volume5
Issue number9
DOIs
Publication statusPublished - Sep 2006

Fingerprint

Horizontal Gene Transfer
Gene Fusion
Plastid Genomes
Eukaryota
Phylogeny
Genes
Rhodophyta
Ascomycota
Plastids
Toxoplasma
Fungi
Tetrahymena thermophila
Oomycetes
Genome
Diatoms
Basidiomycota
Chlorophyta
Symbiosis
Chloroplasts
Organelles

Keywords

  • phylogenetic tree selection
  • apicomplexan parasites
  • red algae
  • photosynthetic eukaryotes
  • common origin
  • plastids
  • enzyme
  • single
  • chloroplast
  • genome

Cite this

Richards, Thomas A ; Dacks, Joel B ; Campbell, Samantha A ; Blanchard, Jeffrey L ; Foster, Peter G ; McLeod, Rima ; Roberts, Craig W. / Evolutionary origins of the eukaryotic shikimate pathway : gene fusions, horizontal gene transfer, and endosymbiotic replacements. In: Eukaryotic Cell. 2006 ; Vol. 5, No. 9. pp. 1517-1531.
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Evolutionary origins of the eukaryotic shikimate pathway : gene fusions, horizontal gene transfer, and endosymbiotic replacements. / Richards, Thomas A; Dacks, Joel B; Campbell, Samantha A; Blanchard, Jeffrey L; Foster, Peter G; McLeod, Rima; Roberts, Craig W.

In: Eukaryotic Cell, Vol. 5, No. 9, 09.2006, p. 1517-1531.

Research output: Contribution to journalArticle

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T1 - Evolutionary origins of the eukaryotic shikimate pathway

T2 - Eukaryotic Cell

AU - Richards, Thomas A

AU - Dacks, Joel B

AU - Campbell, Samantha A

AU - Blanchard, Jeffrey L

AU - Foster, Peter G

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AU - Roberts, Craig W

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KW - phylogenetic tree selection

KW - apicomplexan parasites

KW - red algae

KW - photosynthetic eukaryotes

KW - common origin

KW - plastids

KW - enzyme

KW - single

KW - chloroplast

KW - genome

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