MBE Advance Access originally published online on April 18, 2007
Molecular Biology and Evolution 2007 24(8):1611-1621; doi:10.1093/molbev/msm075
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Research Articles |
Evolution of the Glucose-6-Phosphate Isomerase: The Plasticity of Primary Metabolism in Photosynthetic Eukaryotes
* Institut für Genetik, Technische Universität Braunschweig, Braunschweig, Germany
Georg-Speyer-Haus, Johann Wolfgang Goethe Universität Frankfurt, Frankfurt am Main, Germany
Département de Biochimie, Université de Montréal, Montréal, Quebec, Canada
E-mail: j.petersen{at}tu-bs.de
Accepted for publication April 2, 2007.
Glucose-6-phosphate isomerase (GPI) has an essential function in both catabolic glycolysis and anabolic gluconeogenesis and is universally distributed among Eukaryotes, Bacteria, and some Archaea. In addition to the cytosolic GPI, land plant chloroplasts harbor a nuclear encoded isoenzyme of cyanobacterial origin that is indispensable for the oxidative pentose phosphate pathway (OPPP) and plastid starch accumulation. We established 12 new GPI sequences from rhodophytes, the glaucophyte Cyanophora paradoxa, a ciliate, and all orders of complex algae with red plastids (haptophytes, diatoms, cryptophytes, and dinoflagellates). Our comprehensive phylogenies do not support previous GPI-based speculations about a eukaryote-to-prokaryote horizontal gene transfer from metazoa to 
-proteobacteria. The evolution of cytosolic GPI is largely in agreement with small subunit analyses, which indicates that it is a specific marker of the host cell. A distinct subtree comprising alveolates (ciliates, apicomplexa, Perkinsus, and dinoflagellates), stramenopiles (diatoms and Phytophthora [oomycete]), and Plantae (green plants, rhodophytes, and Cyanophora) might suggest a common origin of these superensembles. Finally, in contrast to land plants where the plastid GPI is of cyanobacterial origin, chlorophytes and rhodophytes independently recruited a duplicate of the cytosolic GPI that subsequently acquired a transit peptide for plastid import. A secondary loss of the cytosolic isoenzyme and the plastid localization of the single GPI in chlorophycean green algae is compatible with physiological studies. Our findings reveal the fundamental importance of the plastid OPPP for Plantae and document the plasticity of primary metabolism.
Key Words: algal evolution • endosymbioses • gene transfer • glycolysis • oxidative pentose phosphate pathway • plastid metabolism
Martin Embley, Associate Editor