Home LiteratureArticle Details
PMID: 7568085 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

A nuclear gene of eubacterial origin in Euglena gracilis reflects cryptic endosymbioses during protist evolution.

Henze K, Badr A, Wettern M, Cerff R, Martin W

Abstract

Genes for glycolytic and Calvin-cycle glyceraldehyde-3-phosphate dehydrogenase (GAPDH) of higher eukaryotes derive from ancient gene duplications which occurred in eubacterial genomes; both were transferred to the nucleus during the course of endosymbiosis. We have cloned cDNAs encoding chloroplast and cytosolic GAPDH from the early-branching photosynthetic protist Euglena gracilis and have determined the structure of its nuclear gene for cytosolic GAPDH. The gene contains four introns which possess unusual secondary structures, do not obey the GT-AG rule, and are flanked by 2- to 3-bp direct repeats. A gene phylogeny for these sequences in the context of eubacterial homologues indicates that euglenozoa, like higher eukaryotes, have obtained their GAPDH genes from eubacteria via endosymbiotic (organelle-to-nucleus) gene transfer. The data further suggest that the early-branching protists Giardia lamblia and Entamoeba histolytica--which lack mitochondria--and portions of the trypanosome lineage have acquired GAPDH genes from eubacterial donors which did not ultimately give rise to contemporary membrane-bound organelles. Evidence that "cryptic" (possibly ephemeral) endosymbioses during evolution may have entailed successful gene transfer is preserved in protist nuclear gene sequences.

MeSH Terms
Amino Acid Sequence Animals Base Composition Base Sequence Biological Evolution Cell Nucleus/metabolism Consensus Sequence Eubacterium/classification,genetics Euglena gracilis/genetics Eukaryota/classification,genetics Fungi/classification,genetics Genes, Bacterial Glyceraldehyde-3-Phosphate Dehydrogenases/genetics Introns Molecular Sequence Data Multigene Family Nucleic Acid Conformation RNA, Bacterial/chemistry,genetics Sequence Homology, Amino Acid Sequence Homology, Nucleic Acid Symbiosis
Chemicals
RNA, Bacterial Glyceraldehyde-3-Phosphate Dehydrogenases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Henze K
Institut für Genetik, Technische Universität Braunschweig, Federal Republic of Germany.
Badr A
Wettern M
Cerff R
Martin W
References (39)
39 references, click to expand
  1. Structure and expression of Euglena gracilis nuclear rbcS genes encoding the small subunits of the ribulose 1,5-bisphosphate carboxylase/oxygenase: a novel splicing process for unusual intervening sequences?
    J Mol Biol. 1995 Jan 6;245(1):22-33 PMID: 7823317
  2. Molecular characterization of a novel, nuclear-encoded, NAD(+)-dependent glyceraldehyde-3-phosphate dehydrogenase in plastids of the gymnosperm Pinus sylvestris L.
    Plant Mol Biol. 1994 Nov;26(4):1155-66 PMID: 7811973
  3. Of archae and eo: what's in a name?
    Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2421-3 PMID: 7708656
  4. Molecular analysis of glyceraldehyde-3-phosphate dehydrogenase in Trypanoplasma borelli: an evolutionary scenario of subcellular compartmentation in kinetoplastida.
    J Mol Evol. 1995 Apr;40(4):443-54 PMID: 7769620
  5. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica.
    Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6518-21 PMID: 7604025
  6. Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron.
    EMBO J. 1991 Oct;10(10):3073-8 PMID: 1915281
  7. Genetic and biochemical implications of the endosymbiotic origin of the chloroplast.
    J Mol Evol. 1981;17(3):133-9 PMID: 7265265
  8. A comprehensive set of sequence analysis programs for the VAX.
    Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95 PMID: 6546423
  9. 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
  10. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions.
    Mol Biol Evol. 1986 Sep;3(5):418-26 PMID: 3444411
  11. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  12. Characterization of cDNA sequences for LHCI apoproteins in Euglena gracilis: the mRNA encodes a large precursor containing several consecutive divergent polypeptides.
    Mol Gen Genet. 1988 Aug;213(2-3):479-86 PMID: 3141775
  13. Energy metabolism of protozoa without mitochondria.
    Annu Rev Microbiol. 1988;42:465-88 PMID: 3059999
  14. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia.
    Science. 1989 Jan 6;243(4887):75-7 PMID: 2911720
  15. 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
  16. Comparative and functional anatomy of group II catalytic introns--a review.
    Gene. 1989 Oct 15;82(1):5-30 PMID: 2684776
  17. Eight small subunits of Euglena ribulose 1-5 bisphosphate carboxylase/oxygenase are translated from a large mRNA as a polyprotein.
    EMBO J. 1990 Feb;9(2):333-8 PMID: 2105882
  18. Evolutionary transfer of the chloroplast tufA gene to the nucleus.
    Nature. 1990 Mar 15;344(6263):262-5 PMID: 2314461
  19. Self-splicing of group I introns.
    Annu Rev Biochem. 1990;59:543-68 PMID: 2197983
  20. A naturally occurring horizontal gene transfer from a eukaryote to a prokaryote.
    J Mol Evol. 1990 Nov;31(5):383-8 PMID: 2124629
  21. 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
  22. 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
  23. Characterization of a Euglena gene encoding a polyprotein precursor to the light-harvesting chlorophyll a/b-binding protein of photosystem II.
    Plant Mol Biol. 1992 Jan;18(2):287-99 PMID: 1731990
  24. Molecular analysis of the cytosolic and glycosomal glyceraldehyde-3-phosphate dehydrogenase in Leishmania mexicana.
    Mol Biochem Parasitol. 1992 Oct;55(1-2):115-26 PMID: 1435864
  25. Chloroplast group III twintron excision utilizing multiple 5'- and 3'-splice sites.
    EMBO J. 1992 Dec;11(13):5041-50 PMID: 1464326
  26. The four genomes of the alga Pyrenomonas salina (Cryptophyta).
    Biosystems. 1992;28(1-3):69-73 PMID: 1292668
  27. Gene phylogenies and the endosymbiotic origin of plastids.
    Biosystems. 1992;28(1-3):75-90 PMID: 1292669
  28. Molecular evolution. Why introns-in-pieces?
    Nature. 1993 Jul 22;364(6435):289-90 PMID: 8332184
  29. Group II self-splicing introns in bacteria.
    Nature. 1993 Jul 22;364(6435):358-61 PMID: 7687328
  30. Complete sequence of Euglena gracilis chloroplast DNA.
    Nucleic Acids Res. 1993 Jul 25;21(15):3537-44 PMID: 8346031
  31. Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes.
    Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8692-6 PMID: 8378350
  32. The presequence of Euglena LHCPII, a cytoplasmically synthesized chloroplast protein, contains a functional endoplasmic reticulum-targeting domain.
    Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11845-9 PMID: 8265635
  33. A glyceraldehyde-3-phosphate dehydrogenase with eubacterial features in the amitochondriate eukaryote, Trichomonas vaginalis.
    J Mol Evol. 1993 Dec;37(6):631-43 PMID: 8114116
  34. Five identical intron positions in ancient duplicated genes of eubacterial origin.
    Nature. 1994 Jan 27;367(6461):387-9 PMID: 8114942
  35. Protein phylogeny gives a robust estimation for early divergences of eukaryotes: phylogenetic place of a mitochondria-lacking protozoan, Giardia lamblia.
    Mol Biol Evol. 1994 Jan;11(1):65-71 PMID: 8121287
  36. Cloning of Giardia lamblia heat shock protein HSP70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):2895-9 PMID: 8159675
  37. Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga.
    Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3690-4 PMID: 8170970
  38. Testing the exon theory of genes: the evidence from protein structure.
    Science. 1994 Jul 8;265(5169):202-7 PMID: 8023140
  39. Chloroplast and cytosolic triosephosphate isomerases from spinach: purification, microsequencing and cDNA cloning of the chloroplast enzyme.
    Plant Mol Biol. 1994 Dec;26(6):1961-73 PMID: 7858230
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
Published
1995-09-26
Pages
9122-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC40936
Subset
IM
Databases
GENBANK
L21903, L21904, L39772
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: product@genelibs.com