Home LiteratureArticle Details
PMID: 8378350 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 90 ·No. 18 ·1993-09-15 ·Pages 8692-6

Martin W, Brinkmann H, Savonna C, Cerff R

Abstract

Higher plants process two distinct, nuclear gene-encoded glyceraldehyde-3-phosphate dehydrogenase (GAPDH) proteins, a Calvin-cycle enzyme active within chloroplasts and a glycolytic enzyme active within the cytosol. The gene for the chloroplast enzyme was previously suggested to be of endosymbiotic origin. Since the ancestors of plastids were related to cyanobacteria, we have studied GAPDH genes in the cyanobacterium Anabaena variabilis. Our results confirm that the nuclear gene for higher plant chloroplast GAPDH indeed derives from the genome of a cyanobacterium-like endosymbiont. But two additional GAPDH genes were found in the Anabaena genome and, surprisingly, one of these sequences is very similar to nuclear genes encoding the GAPDH enzyme of glycolysis in plants, animals, and fungi. Evidence that the eukaryotic nuclear genes for glycolytic GAPDH, as well as the Calvin-cycle genes, are of eubacterial origin suggests that eukaryotic genomes are more highly chimeric than previously assumed.

Related Genes
GapA GapB GapC gap1 gap2
MeSH Terms
Amino Acid Sequence Anabaena/enzymology,genetics Animals Biological Evolution Blotting, Southern Escherichia coli/enzymology,genetics Genes, Bacterial Genes, Plant Genetic Variation Glyceraldehyde-3-Phosphate Dehydrogenases/genetics Glycolysis Humans Molecular Sequence Data Multigene Family Phylogeny Sequence Homology, Amino Acid
Chemicals
Glyceraldehyde-3-Phosphate Dehydrogenases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Martin W
Institut für Genetik, Technische Universität Braunschweig, Germany.
Brinkmann H
Savonna C
Cerff R
References (40)
40 references, click to expand
  1. Genetic and biochemical implications of the endosymbiotic origin of the chloroplast.
    J Mol Evol. 1981;17(3):133-9 PMID: 7265265
  2. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes.
    Mol Biol Evol. 1985 Mar;2(2):150-74 PMID: 3916709
  3. Nucleotide polymorphism and evolution in the glyceraldehyde-3-phosphate dehydrogenase gene (gapA) in natural populations of Salmonella and Escherichia coli.
    Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6667-71 PMID: 1862091
  4. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  5. Molecular phylogenies in angiosperm evolution.
    Mol Biol Evol. 1993 Jan;10(1):140-62 PMID: 8095691
  6. Sequence comparison of glyceraldehyde-3-phosphate dehydrogenases from the three urkingdoms: evolutionary implication.
    Can J Microbiol. 1989 Jan;35(1):81-5 PMID: 2497945
  7. The Deinococcus-Thermus phylum and the effect of rRNA composition on phylogenetic tree construction.
    Syst Appl Microbiol. 1989;11:128-34 PMID: 11542160
  8. Different fates of the chloroplast tufA gene following its transfer to the nucleus in green algae.
    Proc Natl Acad Sci U S A. 1990 Jul;87(14):5317-21 PMID: 2371274
  9. A new approach for molecular cloning in cyanobacteria: cloning of an Anacystis nidulans met gene using a Tn901-induced mutant.
    Gene. 1982 Nov;20(1):111-9 PMID: 6298064
  10. Glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic archaebacterium Pyrococcus woesei: characterization of the enzyme, cloning and sequencing of the gene, and expression in Escherichia coli.
    J Bacteriol. 1990 Aug;172(8):4329-38 PMID: 2165475
  11. Primary structure of glyceraldehyde-3-phosphate dehydrogenase deduced from the nucleotide sequence of the thermophilic archaebacterium Methanothermus fervidus.
    Gene. 1988 Apr 29;64(2):189-97 PMID: 2841192
  12. Metabolism of glucose by unicellular blue-green algae.
    Arch Mikrobiol. 1972;87(4):303-22 PMID: 4629415
  13. Nucleotide sequence of the glyceraldehyde-3-phosphate dehydrogenase gene from the mesophilic methanogenic archaebacteria Methanobacterium bryantii and Methanobacterium formicicum. Comparison with the respective gene structure of the closely related extreme thermophile Methanothermus fervidus.
    Eur J Biochem. 1989 Feb 1;179(2):405-13 PMID: 2492940
  14. Identification, molecular cloning and sequence analysis of a gene cluster encoding the class II fructose 1,6-bisphosphate aldolase, 3-phosphoglycerate kinase and a putative second glyceraldehyde 3-phosphate dehydrogenase of Escherichia coli.
    Mol Microbiol. 1989 Jun;3(6):723-32 PMID: 2546007
  15. Differential intron loss and endosymbiotic transfer of chloroplast glyceraldehyde-3-phosphate dehydrogenase genes to the nucleus.
    Proc Natl Acad Sci U S A. 1990 Nov;87(22):8918-22 PMID: 2247465
  16. Nucleotide sequence of the Escherichia coli gap gene. Different evolutionary behavior of the NAD+-binding domain and of the catalytic domain of D-glyceraldehyde-3-phosphate dehydrogenase.
    Eur J Biochem. 1985 Jul 1;150(1):61-6 PMID: 2990926
  17. Evolution of glycolysis.
    Prog Biophys Mol Biol. 1993;59(2):105-235 PMID: 8426905
  18. Intron conservation across the prokaryote-eukaryote boundary: structure of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2672-6 PMID: 3357887
  19. Bacterial evolution.
    Microbiol Rev. 1987 Jun;51(2):221-71 PMID: 2439888
  20. Fine structural features of the chloroplast genome: comparison of the sequenced chloroplast genomes.
    Nucleic Acids Res. 1991 Mar 11;19(5):983-95 PMID: 1708498
  21. Prokaryotic features of a nucleus-encoded enzyme. cDNA sequences for chloroplast and cytosolic glyceraldehyde-3-phosphate dehydrogenases from mustard (Sinapis alba).
    Eur J Biochem. 1986 Sep 1;159(2):323-31 PMID: 3530755
  22. Sequence and structure of D-glyceraldehyde 3-phosphate dehydrogenase from Bacillus stearothermophilus.
    Nature. 1977 Mar 24;266(5600):328-33 PMID: 193030
  23. Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes.
    Proc Natl Acad Sci U S A. 1989 Dec;86(23):9355-9 PMID: 2531898
  24. A naturally occurring horizontal gene transfer from a eukaryote to a prokaryote.
    J Mol Evol. 1990 Nov;31(5):383-8 PMID: 2124629
  25. Nucleotide sequence of a DNA region comprising the gene for elongation factor 1 alpha (EF-1 alpha) from the ultrathermophilic archaeote Pyrococcus woesei: phylogenetic implications.
    J Mol Evol. 1991 Oct;33(4):332-42 PMID: 1723106
  26. Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes.
    Proc Natl Acad Sci U S A. 1989 Sep;86(17):6661-5 PMID: 2528146
  27. Endosymbiotic origin and codon bias of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize.
    J Mol Evol. 1987;26(4):320-8 PMID: 3131533
  28. Characterization of two D-glyceraldehyde-3-phosphate dehydrogenases from the extremely thermophilic archaebacterium Thermoproteus tenax.
    Eur J Biochem. 1987 Dec 30;170(1-2):325-33 PMID: 3121324
  29. Evidence in favor of the symbiotic origin of chloroplasts: primary structure and evolution of tobacco glyceraldehyde-3-phosphate dehydrogenases.
    Cell. 1986 Oct 10;47(1):73-80 PMID: 3757034
  30. Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome.
    Proc Natl Acad Sci U S A. 1989 Jun;86(12):4569-73 PMID: 2499884
  31. A comprehensive set of sequence analysis programs for the VAX.
    Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95 PMID: 6546423
  32. Phylogenetic analysis of the RNA polymerases of Trypanosoma brucei, with special reference to class-specific transcription.
    Curr Genet. 1990 Dec;18(6):547-51 PMID: 2076555
  33. Protein transport into and within chloroplasts.
    Trends Biochem Sci. 1990 Feb;15(2):73-6 PMID: 2186519
  34. The cytosolic and glycosomal isoenzymes of glyceraldehyde-3-phosphate dehydrogenase in Trypanosoma brucei have a distant evolutionary relationship.
    Eur J Biochem. 1991 Jun 1;198(2):421-8 PMID: 2040303
  35. Disparate evolution of yeasts and filamentous fungi indicated by phylogenetic analysis of glyceraldehyde-3-phosphate dehydrogenase genes.
    Proc Natl Acad Sci U S A. 1989 Sep;86(18):7063-6 PMID: 2674943
  36. Probing the coenzyme specificity of glyceraldehyde-3-phosphate dehydrogenases by site-directed mutagenesis.
    Biochemistry. 1990 Jul 31;29(30):7101-6 PMID: 2223764
  37. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions.
    Mol Biol Evol. 1986 Sep;3(5):418-26 PMID: 3444411
  38. Conservation and duplication of isozymes in plants.
    Science. 1982 Apr 23;216(4544):373-80 PMID: 17745860
  39. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya.
    Proc Natl Acad Sci U S A. 1990 Jun;87(12):4576-9 PMID: 2112744
  40. Evolution of RNA polymerases and branching patterns of the three major groups of Archaebacteria.
    J Mol Evol. 1991 Jan;32(1):70-8 PMID: 1901370
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.90.18.8692
Published
1993-09-15
Pages
8692-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC47424
Subset
IM
Databases
GENBANK
L07497, L07498, L07499
External Links
PubMed source DOI: 10.1073/pnas.90.18.8692 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2