Complete nucleotide sequences of the genes encoding translation elongation factors 1α and 2 from a microsporidian parasite, Glugea plecoglossi: Implications for the deepest branching of eukaryotes

Journal of Biochemistry

Volumn 120, Issue 6, 1996, Pages 1095-1103

  Kamaishi, Takashi ^a,b,c   Hashimoto, Tetsuo ^b   Nakamura, Yoshihiro ^a   Masuda, Yutaka ^a   Nakamura, Fuminori ^a   Okamoto, Ken Ichi ^a   Shimizu, Makoto ^c   Hasegawa, Masami ^b  

^a SHOWA UNIVERSITY   (Japan)

^b INSTITUTE OF STATISTICAL MATHEMATICS   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Ancient divergence of eukaryotes; Elongation factor; Glugea plecoglossi; Microsporidians; Mitochondrion lacking protozoa

Indexed keywords

ELONGATION FACTOR 1ALPHA; ELONGATION FACTOR 2;

AMINO ACID SEQUENCE; ARTICLE; GENE SEQUENCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTOZOON; SEQUENCE HOMOLOGY;

ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; EVOLUTION, MOLECULAR; HUMANS; MICROSPORIDA; MOLECULAR SEQUENCE DATA; PEPTIDE ELONGATION FACTOR 1; PEPTIDE ELONGATION FACTOR 2; PEPTIDE ELONGATION FACTORS; PHOSPHOPROTEINS; PHYLOGENY; PROTEIN PROCESSING, POST-TRANSLATIONAL; RESTRICTION MAPPING; RIBONUCLEOPROTEINS; SEQUENCE ANALYSIS, DNA;

EUKARYOTA; GIARDIA INTESTINALIS; GLUGEA PLECOGLOSSI; MICROSPORIDIA; PROTOZOA;

EID: 0030474879     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.jbchem.a021527     Document Type: Article

References (69)

1. Margulis, L. (1970) Origin of Eukaryotic Cells, Yale Univ. Press, New Haven, CT
2. Schwartz, R.M. and Dayhoff, M.O. (1978) Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts. Science 199, 395-403
3. Cavalier-Smith, T. (1987) Eukaryotes with no mitochondria. Nature 326, 332-333
4. Cavalier-Smith, T. (1989) Archaebacteria and archaezoa. Nature 339, 100-101
5. Cavalier-Smith, T. (1993) Kingdom protozoa and its 18 phyla. Microbiol. Rev. 57, 953-994
6. Sogin, M.L. (1991) Early evolution and the origin of eukaryotes. Curr. Opin. Genet. Dev. 1, 457-463
7. Sogin, M.L. (1994) The origin of eukaryotes and evolution into major kingdoms in Early Life on Earth. Nobel Symposium No. 84 (Bengston, S., ed.) pp. 181-192, Columbia University Press, New York
8. Sogin, M.L., Gunderson, J.H., Elwood, H.J., Alonso, R.A., and Peattie, D.A. (1989) Phylogenetic meaning of the kingdom concept: An unusual ribosomal RNA from Giardia lamblia. Science 243, 75-77
9. + of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol. Biochem. Parasitol. 59, 41-48
10. Hasegawa, M. and Hashimoto, T. (1993) Ribosomal RNA trees misleading? Nature 361, 23
11. Hasegawa, M., Hashimoto, T., and Adachi, J. (1992) Origin and evolution of eukaryotes as inferred from protein sequence data in The Origin and Evolution of the Cell (Haryman, H. and Matsuno, K., eds.) pp. 107-130, World Scientific, Singapore
12. Hashimoto, T., Adachi, J., and Hasegawa, M. (1992) Phylogenetic place of Giardia lamblia, a protozoan that lacks mitochondria. Endocytobiosis Cell Res. 9, 59-69
13. Hashimoto, T., Nakamura, Y., Nakamura, F., Shirakura, T., Adachi, J., Goto, N., Okamoto, K., and Hasegawa, M. (1994) Protein phylogeny gives a robust estimation for early divergences of eukaryotes: Phylogenetic place of a mitochondria-lacking protozoan, Giardia lamblia. Mol. Biol. Evol. 11, 65-71
14. Shirakura, T., Hashimoto, T., Nakamura, Y., Kamaishi, T., Cao, Y., Adachi, J., Hasegawa, M., Yamamoto, A., and Goto, N. (1994) Phylogenetic place of a mitochondria-lacking protozoan, Entamoeba histolytica, inferred from amino acid sequences of elongation factor 2. Jpn. J. Genet. 69, 119-135
15. Hashimoto, T., Nakamura, Y., Kamaishi, T., Adachi, J., Nakamura, F., Okamoto, K., and Hasegawa, M. (1995) Phylogenetic place of kinetoplastid protozoa inferred from a protein phylogeny of elongation factor 1α. Mol. Biochem. Parasitol. 70, 181-185
16. Hashimoto, T., Nakamura, Y., Kamaishi, T., Nakamura, F., Adachi, J., Okamoto, K., and Hasegawa, M. (1995) Phylogenetic place of mitochondrion-lacking protozoan, Giardia lamblia, inferred from amino acid sequences of elongation factor 2. Mol. Biol. Evol. 12, 782-793
17. Kamaishi, T., Hashimoto, T., Nakamura, Y., Nakamura, F., Murata, S., Okada, N., Okamoto, K., Shimizu, M., and Hasegawa, M. (1996) Protein phylogeny of translation elongation factor EF-1α suggests microsporidians are extremely ancient eukaryotes. J. Mol. Evol. 42, 257-263
18. Lom, J. and Dyková, I. (1992) Protozoan Parasites of Fishes, Elsevier, Amsterdam
19. Takvorian, P.M. and Cali, A. (1994) Enzyme histochemical identification of the Golgi apparatus in the microsporidian, Glugea stephani. J. Euk. Microbiol. 41 (Suppl), 63S-64S
20. Ishihara, R. and Hayashi, Y. (1968) Some properties of ribosomes from the sporoplasm of Nosema bombycis. J. Invert. Pathol 11, 377-385
21. Vossbrinck, C.R. and Woese, C.R. (1986) Eukaryotic ribosomes that lack a 5.8S RNA. Nature 320, 287-288
22. Takahashi, S. and Egusa, S. (1977) Studies on Glugea infection of the Ayu, Plecoglossus altivelis - I. Description of the Glugea and a proposal of a new species, Glugea plecoglossi (in Japanese). Fish Pathol. 11, 175-182
23. Merrick, W.C. (1992) Mechanism and regulation of eukaryotic protein synthesis. Microbiol. Rev. 56, 291-315
24. Miyata, T., Iwabe, N., Kuma, K., Kawanishi, Y., Hasegawa, M., Kishino, H., Mukohata, Y., Ihara, K., and Osawa, S. (1991) Phylogenetic relationships among archaebacteria, eubacteria, and eukaryotes in Evolution of Life: Fossils, Molecules, and Culture (Osawa, S. and Honjo, T., eds.) pp. 337-351, Springer-Verlag, Tokyo
25. Hasegawa, M., Hashimoto, T., Adachi, J., Iwabe, N., and Miyata, T. (1993) Early branchings in the evolution of eukaryotes: Ancient divergence of Entamoeba that lacks mitochondria reveal-ed by protein sequence data. J. Mol. Evol. 36, 380-388
26. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor
27. Thorne, J.L., Kishino, H., and Felsenstein, J. (1991) An evolutionary model for maximum likelihood alignment of DNA sequences. J. Mol. Evol. 33, 114-124
28. Thorne, J.L., Kishino, H., and Felsenstein, J. (1992) Inching toward reality: An improved likelihood model of sequence evolution. J. Mol. Evol. 34, 3-16
29. Thorne, J.L. and Churchill, G.A. (1995) Estimation and reliability of molecular sequence alignments. Biometrics 51, 100-113
30. Kishino, H., Miyata, T., and Hasegawa, M. (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J. Mol. Evol. 31, 151-160
31. Cao, Y., Adachi, J., Yano, T., and Hasegawa, M. (1994) Phylogenetic place of guinea pigs: No support of the rodent-polyphyly hypothesis from maximum-likelihood analyses of multiple protein sequences. Mol. Biol. Evol. 11, 593-604
32. Cao, Y., Adachi, J., Janke, A., Pääbo, S., and Hasegawa, M. (1994) Phylogenetic relationships among eutherian orders estimated from inferred sequences of mitochondrial proteins: instability of a tree based on a single gene. J. Mol. Evol. 39, 519-527
33. Adachi, J. (1995) Modeling of Molecular Evolution and Maximum Likelihood Inference of Molecular Phylogeny. Ph D Thesis of the Graduate University for Advanced Studies, The Institute of Statistical Mathematics, Tokyo
34. Adachi, J. and Hasegawa, M. (1996) Computer Science Monographs, No. 28, MOLPHY Version 2.3: Programs for Molecular Phylogenetics Based on Maximum Likelihood. The Institute of Statistical Mathematics, Tokyo
35. Saitou, N. and Nei, M. (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425
36. Price, N.T., Redpath, N.T., Severinov, K.V., Campbell, D.G., Russell, J.M., and Proud, C.G. (1991) Identification of the phosphorylation sites in elongation factor-2 from rabbit reticulocytes. FEBS Lett. 282, 253-258
37. Guillot, D., Penin, F., Di Pietro, A., Sontag, B., Lavergne, J.-P., and Reboud, J.-P. (1993) GTP binding to elongation factor eEF-2 unmasks a tryptophan residue required for biological activity. J. Biol. Chem. 268, 20911-20916
38. 221 is involved in the protective effect of elongation factor eEF-2 on the ricin/α-sarcin site of the ribosome. J. Biol. Chem. 268, 26082-26084
39. Kohno, K., Uchida, T., Ohkubo, H., Nakanishi, S., Nakanishi, T., Fukui, T., Ohtsuka, E., Ikehara, M., and Okada, Y. (1986) Amino acid sequence of mammalian elongation factor 2 deduced from the cDNA sequence: Homology with GTP-binding proteins. Proc. Natl. Acad. Sci. USA 83, 4978-4982
40. Van Ness, B.G., Howard, J.B., and Bodley, J.W. (1980) ADP. ribosylation of elongation factor 2 by diphtheria toxin. J. Biol. Chem. 255, 10710-10716
41. Nilsson, L. and Nygård, O. (1985) Localization of the sites of ADP-ribosylation and GTP binding in the eukaryotic elongation factor EF-2. Eur. J. Biochem. 148, 299-304
42. Nakamura, Y., Hashimoto, T., Kamaishi, T., Adachi, J., Nakamura, F., Okamoto, K., and Hasegawa, M. (1996) Phylogenetic position of kinetoplastid protozoa inferred from the protein phylogenies of elongation factors 1α and 2. J. Biochem. 119, 70-79
43. Toda, K., Tasaka, M., Mashima, K., Kohno, K., Uchida, T., and Takeuchi, I. (1989) Structure and expression of elongation factor 2 gene during development of Dictyostelium discoideum. J. Biol. Chem. 264, 15489-15493
44. Hasegawa, M. and Fujiwara, M. (1993) Relative efficiencies of maximum likelihood, maximum parsimony, and neighbor-joining methods for estimating protein phylogeny. Mol. Phylogenet. Evol. 2, 1-5
45. Wilson, P.G. and Culbertson, M.R. (1988) SUF12 supressor protein of yeast: A fusion protein related to the EF-1 family. J. Mol. Biol. 199, 559-573
46. 1-to-S transition encodes a protein containing an A-kinase target site and GTPase domain. EMBO J. 7, 1175-1182
47. Hoshino, S., Miyazawa, H., Enomoto, T., Hanaoka, F., Kikuchi, Y., Kikuchi, A., and Ui, M. (1989) A human homologue of the yeast GST1 gene codes for a GTP-binding protein and is expressed in a proliferation-dependent manner in mammalian cells. EMBO J. 8, 3807-3814
48. Nelson, R.J., Ziegelhoffer, T., Nicolet, C., Werner-Washburne, M., and Craig, E.A. (1992) The translation machinary and 70 kd heat shock protein cooperate in protein synthesis. Cell 71, 97-105
49. Leyh, T.S., Vogt, T.F., and Suo, Y. (1992) The DNA sequence of the sulfate activation locus from Escherichia coli K-12. J. Biol. Chem. 267, 10405-10410
50. Cervantes, E., Sharma, S.B., Maillet, F., Vasse, J., and Truchet, G. (1989) The Rhizobium meliloti host-range nodQ gene encodes a protein which shares homology with translation elongation and initiation factors. Mol. Microbiol. 3, 745-755
51. Vieille, C. and Elmerich, C. (1990) Characterization of two Azospirillum brasilense Sp7 plasmid genes homologous to Rhizobium, meliloti nodPQ. Mol. Plant Microbe. Interact. 3, 389-400
52. Rivera, M.C. and Lake, J.A. (1992) Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257, 74-76
53. Hashimoto, T. and Hasegawa, M. (1996) Origin and early evolution of eukaryotes inferred from the amino acid sequences of translation elongation factors 1α/Tu and 2/G. Adv. Biophys. 32, 73-120
54. Baldauf, S.L., Palmer, J.D., and Doolittle, W.F. (1996) The root of the universal tree and the origin of eukaryotes based on elongation factor phylogeny. Proc. Natl. Acad. Sci. USA 93, 7749-7754
55. Condeelis, J. (1995) Elongation factor 1α, translation and the cytoskeleton. Trends Biochem. Sci. 20, 169-170
56. Sandstrom, P., Lira, L.M., Choi, D., Linz, J.E., and Sypherd, P.S. (1987) Sequence analysis of the EF-1α gene family of Mucor racemosus. Nucleic Acids Res. 23, 9997-10005
57. Linz, J.E. and Sypherd, P.S. (1987) Expression of three genes for elongation factor 1α during morphogenesis of Mucor racemosus. Mol. Cell Biol. 7, 1925-1932
58. Walldorf, U., Hovemann, B., and Bautz, E.K.F. (1985) F1 and F2: Two similar genes regulated differently during development of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 82, 5795-5799
59. Hovemann, B., Richter, S., Walldorf, U., and Cziepluch, C. (1988) Two genes encode related cytoplasmic elongation factors 1α (EF-1α) in Drosophila melanogaster with continuous and stage specific expression. Nucleic Acids Res. 16, 3175-3194
60. Krieg, P.A., Varnum, S.M., Wormington, W.M., and Melton, D.A. (1989) The mRNA encoding elongation factor 1-α (EF-1α) is a major transcript at the midblastula transition in Xenopus. Dev. Biol. 133, 93-100
61. Djé, M.K., Mazabraud, A., Viel, A., le Marie, M., Denis, H., Crawford, E., and Brown, D.D. (1990) Three genes under different developmental control encode elongation factor 1-α in Xenopus laevis. Nucleic Acids Res. 18, 3489-3493
62. Coppard, N.J., Poulsen, K., Madsen, H.O., Frydenberg, J., and Clark, B.F.C. (1991) 42Sp48 in previtellogenic Xenopus oocytes is structurally homologous to EF-1α and may be a stage-specific elongation factor. J. Cell Biol. 112, 237-243
63. Ann, D.K., Lin, H.H., Lee, S., Tu, Z.-J., and Wang, E. (1992) Characterization of the statin-like S1 and rat elongation factor 1α as two distinctly expressed messages in rat. J. Biol. Chem. 267, 699-703
64. Lee, S., Wolfraim, L.A., and Wang, E. (1993) Differential expression of S1 and elongation factor-1α during rat development. J. Biol. Chem. 268, 24453-24459
65. Perentesis, J.P., Phan, L.D., Gleason, W.B., LaPorte, D.C., and Livingston, D.M. (1992) Saccharomyces cerevisiae elongation factor 2: genetic cloning, characterization of expression, and G-domain modeling. J. Biol. Chem. 267, 1190-1197
66. Clark, C.G. and Roger, A.J. (1995) Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc. Natl. Acad. Sci. USA 92, 6518-6521
67. Brown, J.R. and Doolittle, W.F. (1995) Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications. Proc. Natl. Acad. Sci. USA 92, 2441-2445
68. Yamamoto, A., Hashimoto, T., Asaga, E., Hasegawa, M., and Goto, N. (1996) Phylogenetic position of mitochondrion-lacking protozoan, Trichomonas tenax, based on amino acid sequences of elongation factors 1α and 2. J. Mol. Evol., in press
69. Cai, J., Collins, M.D., McDonald, V., and Thompson, D.E. (1992) PCR cloning and nucleotide sequence determination of the 18S rRNA genes and internal transcribed spacer 1 of the protozoan parasites Cryptosporidium parvum and Cryptosporidium muris. Biochim. Biophys. Acta 1131, 317-320