An Enigmatic GAPDH Gene in the Symbiotic Dinoflagellate Genus Symbiodinium and its Related Species (the Order Suessiales): Possible Lateral Gene Transfer between Two Eukaryotic Algae, Dinoflagellate and Euglenophyte

Protist

Volumn 154, Issue 3-4, 2003, Pages 443-454

  Takishita, Kiyotaka ^a,c   Ishida, Ken Ichiro ^b   Maruyama, Tadashi ^a,c  

^a MARINE BIOTECHNOLOGY INSTITUTE   (Japan)

^b KANAZAWA UNIVERSITY   (Japan)

^c JAPAN AGENCY FOR MARINE EARTH SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAE; DINOPHYCEAE; EUGLENA; EUGLENA GRACILIS; EUGLENIDA; EUKARYOTA; GYMNODINIUM; GYMNODINIUM SIMPLEX; KINETOPLASTIDA; POLARELLA GLACIALIS; PYROCYSTIS; SUESSIALES; SYMBIODINIUM;

EID: 0242625274     PISSN: 14344610     EISSN: None     Source Type: Journal    
DOI: 10.1078/143446103322454176     Document Type: Article

References (42)

1. Archibald JM, Rogers MB, Toop M, Ishida K, Keeling PJ (2003) Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga, Bigelowiella natans. Proc Natl Acad Sci USA 100: 7678-7683
2. Baillie BK, Belda-Baillie CA, Maruyama T (2000) Conspecificity and Indo-Pacific distribution of Symbiodinium genotypes (Dinophyceae) from giant clams. J Phycol 36: 1153-1161
3. Brinkmann H, Cerff R, Salomon M, Soll J (1989) Cloning and sequence analysis of cDNAs encoding the cytosolic precursors of subunits GapA and GapB of chloroplast glyceraldehyde-3-phosphate dehydrogenase from pea and spinach. Plant Mol Biol 13: 81-94
4. Carlos AA, Baillie BK, Kawachi M, Maruyama T (1999) Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain. J Phycol 35: 1054-1062
5. Clermont S, Corbier C, Mely Y, Gerard D, Wonacott A, Branlant G (1993) Determinants of coenzyme specificity in glyceraldehyde-3-phosphate dehydrogenase: role of the acidic residue in the fingerprint region of the nucleotide binding fold. Biochemistry 32: 10178-10184
6. Daugbjerg N, Hansen G, Larsen J, Moestrup Ø (2000) Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of 3 new genera of unarmoured dinoflagellates. Phycologia 39: 302-317
7. Deane JA, Fraunholz M, Su V, Maier U-G, Martin W, Durnford DG, McFadden GI (2000) Evidence for nucleomorph to host nucleus gene transfer: light-harvesting complex proteins from cryptomonads and chlorarachniophytes. Protist 151: 239-252
8. Doolittle WF (1999a) Lateral genomics. Trends Cell Biol 9: M5-M8
9. Doolittle WF (1999b) Phylogenetic classification and the universal tree. Science 284: 2124-2129
10. Fagan TF, Hastings WJ (2002) Phylogenetic analysis indicates multiple origins of chloroplast glyceraldehyde-3-phosphate dehydrogenase genes in dinoflagellates. Mol Biol Evol 19: 1203-1207
11. Fagan T, Hastings WJ, Morse D (1998) The phylogeny of glyceraldehyde-3-phosphate dehydrogenase indicates lateral gene transfer from cryptomonads to dinoflagellates. J Mol Evol 47: 633-639
12. Fast NM, Kissinger JC, Roos DS, Keeling PJ (2001) Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol Biol Evol 18: 418-426
13. Felsenstein J (1995) PHYLIP, Phylogeny Inference Package (Department of Genetics, Univ. of Washington, Seattle), Version 3.57c
14. Felsenstein J (2001) PHYLIP, Phylogeny Inference Package (Department of Genetics, Univ. of Washington, Seattle), Version 3.6a2
15. Fensome RA, Taylor FJR, Norris G, Sarjeant WAS, Wharton DI, Williams GL, eds (1993) A Classification of Living and Fossil Dinoflagellates: Micropaleontology, Special Publication No. 7. Sheridan Press, Hanover, Pennsylvania
16. Figge RM, Cerff R (2001) GAPDH gene diversity in spirochetes: a paradigm for genetic promiscuity. Mol Biol Evol 18: 2240-2249
17. Figge RM, Schubert M, Brinkmann H, Cerff R (1999) Glyceraldehyde-3- phosphate dehydrogenase gene diversity in eubacteria and eukaryotes: evidence for intra-and inter-kingdom gene transfer. Mol Biol Evol 16: 429-440
18. Henze K, Badr A, Wettern M, Cerff R, Martin W (1995) A nuclear gene of eubacterial origin in Euglena gracilis reflects cryptic endosymbioses during protist evolution. Proc Natl Acad Sci USA 92: 9122-9126
19. Ishida K, Green BR (2002) Second-and third-hand chloroplasts in dinoflagellates: phytogeny of oxygen-evolving enhancer 1 (PsbO) protein reveals replacement of a nuclear-encoded plastid gene by that of a haptophyte tertiary endosymbiont. Proc Natl Acad Sci USA 99: 9294-9299
20. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. CABIOS 8: 275-282
21. Katz LA (2002) Lateral gene transfers and the evolution of eukaryotes: theories and data. Int J Syst Evol Microbiol 52: 1893-1900
22. Keeling PJ, Palmer JD (2001) Lateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase. Proc Natl Acad Sci USA 98: 10745-10750
23. Lake JA, Jain R, Rivera MC (1999) Mix and match in the tree of life. Science 283: 2027-2028
24. Lambeir AM, Loiseau AM, Kuntz DA, Vellieux FM, Michels PA, Opperdoes FR (1991) The cytosolic and glycosomal glyceraldehyde-3-phosphate dehydrogenase from Trypanosoma brucei. Kinetic properties and comparison with homologous enzymes. Eur J Biochem 198: 429-435
25. Liaud MF, Brandt U, Scherzinger M, Cerff R (1997) Evolutionary origin of cryptomonad microalgae: two novel chloroplast/cytosol-specific GAPDH genes as potential markers of ancestral endosymbiont and host cell components. J Mol Evol 44 (Suppl.): S28-S37
26. Liaud MF, Lichtle 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 g lycolytic pathway. Mol Biol Evol 17: 213-223
27. Liaud MF, Valentin C, Martin W, Bouget FY, Kloareg B, Cerff R (1994) The evolutionary origin of red algae as deduced from the nuclear genes encoding cytosolic and chloroplast glyceraldehyde-3-phosphate dehydrogenases from Chondrus crispus. J Mol Evol 38: 319-327
28. Martin W, Brinkmann H, Savonna C, Cerff R (1993) Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3- phosphate dehydrogenase genes. Proc Natl Acad Sci USA 90: 8692-8696
29. Montresor M, Procaccini G, Stoecker DK (1999) Polarella glacialis gen. nov., sp. nov. (Dinophyceae): Suessiaceae are still alive! J Phycol 35: 186-197
30. Qian Q, Keeling PJ (2001) Diplonemid glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and prokaryoteto-eukaryote lateral gene transfer. Protist 152: 193-201
31. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425
32. Saldarriaga JF, Taylor FJ, Keeling PJ, Cavalier-Smith T (2001) Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J Mol Evol 53: 204-213
33. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504
34. Smith TL (1989) Disparate evolution of yeasts and filamentous fungi indicated by phylogenetic analysis of glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci USA 86: 7063-7066
35. Takishita K, Ishikura M, Koike K, Maruyama T (2003) Comparison of phylogenies based on nuclear-encoded SSU rDNA and plastid-encoded psbA in the symbiotic dinoflagellate genus Symbiodinium. Phycologia 42: 285-291
36. Takishita K, Uchida A (1999) Molecular cloning and nucleotide sequence analysis of psbA from the dinoflagellates: Origin of the dinoflagellate plastid. Phycol Res 47: 207-216
37. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weight-ing, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680
38. Viscogliosi E, Muller M (1998) Phylogenetic relationships of the glycolytic enzyme, glyceraldehyde-3-phosphate dehydrogenase, from parabasalid flagellates. J Mol Evol 47: 190-199
39. Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18: 691-699
40. Yoon HS, Hackett JD, Bhattacharya D (2002) A single origin of the peridinin-and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc Natl Acad Sci USA 99: 11724-11729
41. Zhang Z, Green BR, Cavalier-Smith T (1999) Single gene circles in dinoflagellate chloroplast genomes. Nature 400: 155-159
42. Zhang Z, Green BR, Cavalier-Smith T (2000) Phylogeny of ultra-rapidly evolving dinoflagellate chloroplast genes: a possible common origin for sporozoan and dinoflagellate plastids. J Mol Evol 51: 26-40