The evolution and compartmentation of biochemical pathways in eukaryotes

Using a straightforward gene-for-gene approach, we have studied the evolutionary history of (all of) the enzymes of the Calvin cycle, glycolysis, gluconeogenesis, the citric acid cycle in higher plants. We have also studied the evolution of some other pathways, including the mevanolate and deoxyxylulose-5-phosphate pathways of isoprene biosynthesis. We have found that all of the nuclear-encoded enzymes involved in central carbon metabolism in higher plants are more similar to their eubacterial homologues than they are to their archaebacterial homologues, the single exception being enolase. Surprisingly, this is true not only for the enzymes localized in organelles, but also for the enzymes localized in the eukaryotic cytosol. Much more surprisingly, also in eukaryotes that lack organelles altogether, the enzymes of primary carbohydrate metabolism are more similar to their eubacterial than to their archaebacterial homologues. Overall, it looks to us as if eukaryotes acquired not only their organelles through endosymbiosis, but also the enzymatic backbone of their heterotrophic lifesytle.

Some papers on this topic are:

  • Lange BM, Rujan T, Martin W, Croteau R (2000) Isoprenoid biosynthesis: The evolution of two ancient and distinct pathways across genomes. Proc. Natl. Acad. Sci. USA 97:13172–13177.
  • Schnarrenberger C, Martin W (2002) Evolution of the enzymes of the citric acid cycle and the glyoxylate cycle of higher plants: A case study of endosymbiotic gene transfer. Eur. J. Biochem. 269:868–883.
  • Krepinsky K, Plaumann M, Martin W, Schnarrenberger C (2001) Purification and cloning of chloroplast 6-phosphogluconate dehydrogenase from spinach: Cyanobacterial genes for chloroplast and cytosolic isoenzymes encoded in eukaryotic chromosomes. Eur. J. Biochem. 268: 2678–2686.
  • Hannaert V, Brinkmann H, Nowitzki U, Lee JA, Albert M-A, Sensen C, Gaasterland T, Müller M, Michels P, Martin W (2000) 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. 17:989–1000.
  • Liaud M-F, Lichtlé C, Apt K, Martin W, Cerff R (2000) 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. Mol. Biol. Evol. 17: 213–223.
  • Martin W, Scheibe R, Schnarrenberger C (2000) The Calvin cycle and its regulation. In Advances in Photosynthesis Vol. 9. R.C. Leegood, T.D. Sharkey, S. von Caemmerer (eds). Kluwer Academic Publishers. pp. 9–51.
  • Flechner A, Gross W, Martin W, Schnarrenberger C (1999) Chloroplast class I and class II aldolases are bifunctional for fructose-1,6-bisphosphate and sedoheptulose-1,7-bisphosphate cleavage in the Calvin cycle. FEBS Lett. 447:200–202.
  • Nowitzki U, Flechner A, Kellermann J, Hasegawa M, Schnarrenberger C, Martin W (1998) Eubacterial origin of eukaryotic nuclear genes for chloroplast and cytosolic glucose-6-phosphate isomerase: Sampling eubacterial gene diversity in eukaryotic chromosomes through symbiosis. Gene 214:205–213.
  • Meyer-Gauen G, Herbrand H, Pahnke J, Cerff R, Martin W (1998) Gene structure, expression in Escherichia coli and biochemical properties of the NAD+-dependent glyceraldehyde-3-phosphate dehydrogenase from Pinus sylvestris chloroplasts. Gene 209:167–174.
  • Martin W, Schnarrenberger C (1997) The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: A case study of functional redundancy in ancient pathways through endosymbiosis. Curr. Genet. 32:1–18.


Prof. Dr. William F. Martin

Molekulare Evolution
Universitätsstraße 1
Gebäude: 26.13
Etage/Raum: 01.34
Tel.: +49 211 81-13011
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