Molecular Biology and Evolution 17:213-223 (2000)
© 2000 Society for Molecular Biology and Evolution
ARTICLES |
Compartment-Specific Isoforms of TPI and GAPDH are Imported into Diatom Mitochondria as a Fusion Protein: Evidence in Favor of a Mitochondrial Origin of the Eukaryotic Glycolytic Pathway
*Institute of Genetics, University of Braunschweig, Braunschweig, Germany;
Laboratoire de Photorégulation et Dynamique des Membranes Végétales, Ecole Normale Supérieure, Paris, France;
and
Martek Biosciences, Columbia, Maryland
Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and triosephosphate isomerase (TPI) are essential to glycolysis, the major route of carbohydrate breakdown in eukaryotes. In animals and other heterotrophic eukaryotes, both enzymes are localized in the cytosol; in photosynthetic eukaryotes, GAPDH and TPI exist as isoenzymes that function in the glycolytic pathway of the cytosol and in the Calvin cycle of chloroplasts. Here, we show that diatoms—photosynthetic protists that acquired their plastids through secondary symbiotic engulfment of a eukaryotic rhodophyte—possess an additional isoenzyme each of both GAPDH and TPI. Surprisingly, these new forms are expressed as an TPI-GAPDH fusion protein which is imported into mitochondria prior to its assembly into a tetrameric bifunctional enzyme complex. Homologs of this translational fusion are shown to be conserved and expressed also in nonphotosynthetic, heterokont-flagellated oomycetes. Phylogenetic analyses show that mitochondrial GAPDH and its N-terminal TPI fusion branch deeply within their respective eukaryotic protein phylogenies, suggesting that diatom mitochondria may have retained an ancestral state of glycolytic compartmentation that existed at the onset of mitochondrial symbiosis. These findings strongly support the view that nuclear genes for enzymes of glycolysis in eukaryotes were acquired from mitochondrial genomes and provide new insights into the evolutionary history (host-symbiont relationships) of diatoms and other heterokont-flagellated protists.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  C. Grauvogel, H. Brinkmann, and J. Petersen Evolution of the Glucose-6-Phosphate Isomerase: The Plasticity of Primary Metabolism in Photosynthetic Eukaryotes Mol. Biol. Evol., August 1, 2007; 24(8): 1611 - 1621. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Petersen, R. Teich, B. Becker, R. Cerff, and H. Brinkmann The GapA/B Gene Duplication Marks the Origin of Streptophyta (Charophytes and Land Plants) Mol. Biol. Evol., June 1, 2006; 23(6): 1109 - 1118. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Sparla, M. Zaffagnini, N. Wedel, R. Scheibe, P. Pupillo, and P. Trost Regulation of Photosynthetic GAPDH Dissected by Mutants Plant Physiology, August 1, 2005; 138(4): 2210 - 2219. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. K. Michels, N. Wedel, and P. G. Kroth Diatom Plastids Possess a Phosphoribulokinase with an Altered Regulation and No Oxidative Pentose Phosphate Pathway Plant Physiology, March 1, 2005; 137(3): 911 - 920. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Montsant, K. Jabbari, U. Maheswari, and C. Bowler Comparative Genomics of the Pennate Diatom Phaeodactylum tricornutum Plant Physiology, February 1, 2005; 137(2): 500 - 513. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. J. Patron, M. B. Rogers, and P. J. Keeling Gene Replacement of Fructose-1,6-Bisphosphate Aldolase Supports the Hypothesis of a Single Photosynthetic Ancestor of Chromalveolates Eukaryot. Cell, October 1, 2004; 3(5): 1169 - 1175. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. J. Keeling Diversity and evolutionary history of plastids and their hosts Am. J. Botany, October 1, 2004; 91(10): 1481 - 1493. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. T. Harper and P. J. Keeling Nucleus-Encoded, Plastid-Targeted Glyceraldehyde-3-Phosphate Dehydrogenase (GAPDH) Indicates a Single Origin for Chromalveolate Plastids Mol. Biol. Evol., October 1, 2003; 20(10): 1730 - 1735. [Abstract] [Full Text]
|
|
|
|
 |
|
 K. A. Webster Evolution of the coordinate regulation of glycolytic enzyme genes by hypoxia J. Exp. Biol., September 1, 2003; 206(17): 2911 - 2922. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. S. Yoon, J. D. Hackett, G. Pinto, and D. Bhattacharya From the Cover: The single, ancient origin of chromist plastids PNAS, November 26, 2002; 99(24): 15507 - 15512. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. F. Fagan and J. Woodland Hastings Phylogenetic Analysis Indicates Multiple Origins of Chloroplast Glyceraldehyde-3-Phosphate Dehydrogenase Genes in Dinoflagellates Mol. Biol. Evol., July 1, 2002; 19(7): 1203 - 1207. [Full Text] [PDF]
|
|
|
|
|
|
R. M. Figge and R. Cerff GAPDH Gene Diversity in Spirochetes: A Paradigm for Genetic Promiscuity Mol. Biol. Evol., December 1, 2001; 18(12): 2240 - 2249. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. M. Fast, J. C. Kissinger, D. S. Roos, and P. J. Keeling Nuclear-Encoded, Plastid-Targeted Genes Suggest a Single Common Origin for Apicomplexan and Dinoflagellate Plastids Mol. Biol. Evol., March 1, 2001; 18(3): 418 - 426. [Abstract] [Full Text]
|
|
|
|
|
|
V. Hannaert, H. Brinkmann, U. Nowitzki, J. A. Lee, M.-A. Albert, C. W. Sensen, T. Gaasterland, M. M, P. Michels, and W. Martin Enolase from Trypanosoma brucei, from the Amitochondriate Protist Mastigamoeba balamuthi, and from the Chloroplast and Cytosol of Euglena gracilis: Pieces in the Evolutionary Puzzle of the Eukaryotic Glycolytic Pathway Mol. Biol. Evol., July 1, 2000; 17(7): 989 - 1000. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. L. Knowles, C. S. Smith, C. R. Smith, and W. C. Plaxton Structural and Regulatory Properties of Pyruvate Kinase from the Cyanobacterium Synechococcus PCC 6301 J. Biol. Chem., June 8, 2001; 276(24): 20966 - 20972. [Abstract] [Full Text] [PDF]
|
|