Assessing the monophyly of chlorophyll-c containing plastids by multi-gene phylogenies under the unlinked model conditions

Molecular Phylogenetics and Evolution

Volumn 45, Issue 1, 2007, Pages 227-238

  Iida, Kei ^a   Takishita, Kiyotaka ^b   Ohshima, Kazuhiko ^a   Inagaki, Yuji ^c  

^a NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

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

^c UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Chromalveolate; Chromist; Concatenate model; Model misspecification; Secondary endosymbiosis; Separate model

Indexed keywords

CHLOROPHYLL; CHLOROPHYLL C; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CILIATE; CLASSIFICATION; COMPARATIVE STUDY; DINOFLAGELLATE; EVALUATION; GENETICS; MOLECULAR EVOLUTION; MULTIGENE FAMILY; PHYLOGENY; PLASTID;

ANIMALS; CHLOROPHYLL; CILIOPHORA; DINOFLAGELLIDA; EVOLUTION, MOLECULAR; MODELS, BIOLOGICAL; MODELS, GENETIC; MULTIGENE FAMILY; PHYLOGENY; PLASTIDS;

CHROMALVEOLATA; CHROMISTA; CRYPTOPHYTA; DINOPHYCEAE; HAPTOPHYCEAE; STRAMENOPILES;

EID: 34548474869     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2007.05.003     Document Type: Article

References (66)

1. Akaike H. A new look at the statistical model identification. IEEE Trans. Automat. Contr. 19 (1974) 716-723
2. Archibald J.M., and Keeling P.J. Recycled plastids: a 'green movement' in eukaryotic evolution. Trends Genet. 18 (2002) 577-584
3. Archibald J.M., and Keeling P.J. The evolutionary history of plastids: a molecular phylogenetic perspective. In: Hirt R.P., and Horner D.S. (Eds). Organelles, Genomes and Eukaryote Phylogeny: An Evolutionary Synthesis in the Age of Genomics (2004), CRC press, Boca Raton 55-74
4. Archibald J.M., Rogers M.B., Toop M., Ishida K., and Keeling P.J. Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc. Natl. Acad. Sci. USA 100 (2003) 7678-7683
5. Bachvaroff T.R., Concepcion G.T., Rogers C.R., Herman E.M., and Delwiche C.F. Dinoflagellate expressed sequence tag data indicate massive transfer of chloroplast genes to the nuclear genome. Protist 155 (2004) 65-78
6. Bachvaroff T.R., Sanchez Puerta M.V., and Delwiche C.F. Chlorophyll c-containing plastid relationships based on analyses of a multigene data set with all four chromalveolate lineages. Mol. Biol. Evol. 22 (2005) 1772-1782
7. Bhattacharya D., Yoon H.S., and Hackett J.D. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 26 (2004) 50-60
8. Blanchard J.L., and Hicks J.S. The non-photosynthetic plastid in malarial parasites and other apicomplexans is derived from outside the green plastid lineage. J. Eukaryot. Microbiol. 46 (1999) 367-375
9. Bodyl A. Do plastid-related characters support the chromalveolate hypothesis?. J. Phycol. 41 (2003) 712-719
10. Bodyl A., and Mosczyński K. Did the peridinin plastid evolve through tertiary endosymbiosis? A hypothesis. Eur. J. Phycol. 41 (2006) 435-448
11. Cai X., Fuller A.L., McDougald L.R., and Zhu G. Apicoplast genome of the coccidian Eimeria tenella. Gene 321 (2003) 39-46
12. Cao Y., and Hasegawa M. Model misspecification in molecular phylogentic inference as illustrated in evolutionary study of vertebrates. Proc. Inst. Stat. Math. 50 (2002) 69-85
13. Cavalier-Smith T. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryotic family tree. J. Eukaryot. Microbiol. 46 (1999) 347-366
14. Cavalier-Smith T. Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr. Biol. 12 (2002) R62-R64
15. Delwiche C.F. Tracing the thread of plastid diversity through the tapestry of life. Am. Nat. 154 (1999) S164-S177
16. Delwiche C.F., and Palmer J.D. Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol. Biol. Evol. 13 (1996) 873-882
17. Ehara E., Kitayama T., Watanabe K.I., Inagaki Y., Hayashi-lshimaru Y., and Ohama T. Comprehensive molecular phylogenetic analysis of a heterokont alga (NIES 548) using genes from all three cellular compartments. Phycol. Res. 47 (1999) 225-231
18. Ehara M., Hayashi-Ishimaru Y., Inagaki Y., and Ohama T. Use of a deviant mitochondrial genetic code in yellow-green algae as a landmark for segregating members within the phylum. J. Mol. Evol. 45 (1997) 119-124
19. Ehara M., Inagaki Y., Watanabe K.I., and Ohama T. Phylogenetic analysis of diatom coxI genes and implications of a fluctuating GC content on mitochondrial genetic code evolution. Curr. Genet. 37 (2000) 29-33
20. Eisen J.A., Coyne R.S., Wu M., Wu D., Thiagarajan M., Wortman J.R., Badger J.H., Ren Q., Amedeo P., Jones K.M., Tallon L.J., Delcher A.L., Salzberg S.L., Silva J.C., Haas B.J., Majoros W.H., Farzad M., Carlton J.M., Smith R.K., Garg J., Pearlman R.E., Karrer K.M., Sun L., Manning G., Elde N.C., Turkewitz A.P., Asai D.J., Wilkes D.E., Wang Y., Cai H., Collins K., Stewart B.A., Lee S.R., Wilamowska K., Weinberg Z., Ruzzo W.L., Wloga D., Gaertig J., Frankel J., Tsao C.C., Gorovsky M.A., Keeling P.J., Waller R.F., Patron N.J., Cherry J.M., Stover N.A., Krieger C.J., Del Toro C., Ryder H.F., Williamson S.C., Barbeau R.A., Hamilton E.P., and Orias E. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol. 4 (2006)
21. Fast N.M., Kissinger J.C., Roos D.S., and Keeling P.J. Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol. Biol. Evol. 18 (2001) 418-426
22. Felsenstein, J., 1993. PHYLIP: Phylogeny Inference Package Version 3.6. University of Washington, Seattle.
23. Funes S., Davidson E., Reyes-Prieto A., Magallon S., Herion P., King M.P., and Gonzalez-Halphen D. A green algal apicoplast ancestor. Science 298 (2002) 2155
24. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., Carlton J.M., Pain A., Nelson K.E., Bowman S., Paulsen I.T., James K., Eisen J.A., Rutherford K., Salzberg S.L., Craig A., Kyes S., Chan M.S., Nene V., Shallom S.J., Suh B., Peterson J., Angiuoli S., Pertea M., Allen J., Selengut J., Haft D., Mather M.W., Vaidya A.B., Martin D.M., Fairlamb A.H., Fraunholz M.J., Roos D.S., Ralph S.A., McFadden G.I., Cummings L.M., Subramanian G.M., Mungall C., Venter J.C., Carucci D.J., Hoffman S.L., Newbold C., Davis R.W., Fraser C.M., and Barrell B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419 (2002) 498-511
25. Gray M.W., Burger G., and Lang B.F. Mitochondrial evolution. Science 283 (1999) 1476-1481
26. Guindon S., and Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52 (2003) 696-704
27. Hackett J.D., Yoon H.S., Soares M.B., Bonaldo M.F., Casavant T.L., Scheetz T.E., Nosenko T., and Bhattacharya D. Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Curr. Biol. 14 (2004) 213-218
28. Harper J.T., and Keeling P.J. Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol. Biol. Evol. 20 (2003) 1730-1735
29. Harper J.T., Waanders E., and Keeling P.J. On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int. J. Syst. Evol. Microbiol. 55 (2004) 487-496
30. Hashimoto T., Arisue N., and Hasegawa M. Application of molecular phylogenetic inference and associated problems: illustrative data analysis on early eukaryotic evolution. Proc. Inst. Stat. Math. 50 (2002) 45-68
31. Hayashi-Ishimaru Y., Ehara M., Inagaki Y., and Ohama T. A deviant mitochondrial genetic code in prymnesiophytes (yellow-algae): UGA codon for tryptophan. Curr. Genet. 32 (1997) 296-299
32. Inagaki Y., Ehara M., Watanabe K.I., Hayashi-Ishimaru Y., and Ohama T. Directionally evolving genetic code: the UGA codon from stop to tryptophan in mitochondria. J. Mol. Evol. 47 (1998) 378-384
33. Inagaki Y., Hayashi-Ishimaru Y., Ehara M., Igarashi I., and Ohama T. Algae or protozoa: phylogenetic position of euglenophytes and dinoflagellates as inferred from mitochondrial sequences. J. Mol. Evol. 45 (1997) 295-300
34. Inagaki Y., and Roger A.J. Phylogenetic estimation under codon modelscan be biased by codon usage heterogeneity. Mol. Phylogenet. Evol. 40 (2006) 428-434
35. Inagaki Y., Simpson A.G.B., Dacks J.B., and Roger A.J. Phylogenetic artifacts can be caused by leucine, serine, and arginine codon usage heterogeneity: dinoflagellate plastid origins as a case study. Syst. Biol. 53 (2004) 582-593
36. Ishida K., Cao Y., Hasegawa M., Okada N., and Hara Y. The origin of chlorarachniophyte plastids, as inferred from phylogenetic comparisons of amino acid sequences of EF-Tu. J. Mol. Evol. 45 (1997) 682-687
37. Köhler S., Delwiche C.F., Denny P.W., Tilney L.G., Webster P., Wilson R.J., Palmer J.D., and Roos D.S. A plastid of probable green algal origin in apicomplexan parasites. Science 275 (1997) 1485-1489
38. Kolaczkowski B., and Thornton J.W. Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous. Nature 431 (2004) 980-984
39. McFadden G.I., and Waller R.F. Plastids in parasites of humans. Bioessays 19 (1997) 1033-1040
40. Morse D., Salois P., Markovic P., and Hastings J.W. A nuclear-encoded form II RuBisCO in dinoflagellates. Science 268 (1995) 1622-1624
41. Palmer J.D. The symbiotic birth and spread of plastids: how many times and whodunit?. J. Phycol. 39 (2003) 4-11
42. Patron N.J., Inagaki Y., and Keeling P.J. Multiplegene phylogenies support the monophyly of cryptomonad and haptophyte host lineages. Curr. Biol. 17 10 (2007) 887-891
43. Patron N.J., Rogers M.B., and Keeling P.J. Gene replacement of fructose-1,6-bisphosphate aldolase supports the hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryot. Cell 3 (2004) 1169-1175
44. Petersen J., Teich R., Brinkmann H., and Cerff R. A "green" phosphoribulokinase in complex algae with red plastids: evidence for a single secondary endosymbiosis leading to haptophytes, cryptophytes, heterokonts, and dinoflagellates. J. Mol. Evol. 62 (2006) 143-157
45. Posada D., and Crandall K.A. MODELTEST: testing the model of DNA substitution. Bioinformatics 14 (1998) 817-818
46. Pupko T., Huchon D., Cao Y., Okada N., and Hasegawa M. Combining multiple data sets in a likelihood analysis: which models are the best?. Mol. Biol. Evol. 19 (2002) 2294-2307
47. Rice D.W., and Palmer J.D. An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters. BMC Biol. 4 (2006) 31
48. Rodríguez-Ezpeleta N., Brinkmann H., Burey S.C., Roure B., Burger G., Löffelhardt W., Bohnert H.J., Philippe H., and Lang B.F. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr. Biol. 15 (2005) 1325-1330
49. Rogers M.B., Gilson P.R., Su V., McFadden G.I., and Keeling P.J. The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of chlorarachniophyte and euglenid secondary endosymbionts. Mol. Biol. Evol. 24 1 (2007) 54-62
50. Ruiz-Trillo I., Inagaki Y., Davis L.A., Sperstad S., Landfald B., and Roger A.J. Capsaspora owczarzaki is an independent opisthokont lineage. Curr. Biol. 14 (2004) R946-R947
51. Sanchez Puerta, M.V., Bachvaroff, T.R., Delwiche, C.F., in press. Sorting wheat from chaff in multi-gene analyses of Chlorophyll c-containing plastids. Mol. Phylogenet. Evol., doi:10.1016/j.ympev.2007.03.003.
52. Schmidt H.A., Strimmer K., Vingron M., and von Haeseler A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18 (2002) 502-504
53. Shalchian-Tabrizi K., Skanseng M., Ronquist F., Klaveness D., Bachvaroff T.R., Delwiche C.F., Botnen A., Tengs T., and Jakobsen K.S. Heterotachy processes in rhodophyte-derived secondhand plastid genes: Implications for addressing the origin and evolution of dinoflagellate plastids. Mol. Biol. Evol. 23 (2006) 1504-1515
54. Shimodaira H. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51 (2002) 492-508
55. Shimodaira H., and Hasegawa M. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17 (2001) 1246-1247
56. Spencer M., Susko E., and Roger A.J. Likelihood, parsimony, and heterogeneous evolution. Mol. Biol. Evol. 22 (2005) 1161-1164
57. Takishita K., Inagaki Y., Tsuchiya M., Sakaguchi M., and Maruyama T. A close relationship between Cercozoa and Foraminifera supported by phylogenetic analyses based on combined amino acid sequences of three cytoskeletal proteins (actin, α-tubulin, and β-tubulin). Gene 362 (2005) 153-160
58. Takishita K., Ishida K., Ishikura M., and Maruyama T. Phylogeny of the psbC gene, encoding a photosystem II component CP43, suggests separate origins for the peridinin- and the fucoxanthin derivatives-containing plastids of dinoflagellates. Phycologia 44 (2005) 26-34
59. Tyler B.M., Tripathy S., Zhang X., Dehal P., Jiang R.H., Aerts A., Arredondo F.D., Baxter L., Bensasson D., Beynon J.L., Chapman J., Damasceno C.M., Dorrance A.E., Dou D., Dickerman A.W., Dubchak I.L., Garbelotto M., Gijzen M., Gordon S.G., Govers F., Grunwald N.J., Huang W., Ivors K.L., Jones R.W., Kamoun S., Krampis K., Lamour K.H., Lee M.K., McDonald W.H., Medina M., Meijer H.J., Nordberg E.K., Maclean D.J., Ospina-Giraldo M.D., Morris P.F., Phuntumart V., Putnam N.H., Rash S., Rose J.K., Sakihama Y., Salamov A.A., Savidor A., Scheuring C.F., Smith B.M., Sobral B.W., Terry A., Torto-Alalibo T.A., Win J., Xu Z., Zhang H., Grigoriev I.V., Rokhsar D.S., and Boore J.L. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313 (2006) 1261-1266
60. Whitney S.M., Shaw D.C., and Yellowlees D. Evidence that some dinoflagellates contain a ribulose-1,5-bisphosphate carboxylase/oxygenase related to that of the alpha-proteobacteria. Proc. Biol. Sci. 259 (1995) 271-275
61. Williamson D.H., Gardner M.J., Preiser P., Moore D.J., Rangachari K., and Wilson R.J. The evolutionary origin of the 35 kb circular DNA of Plasmodium falciparum: new evidence supports a possible rhodophyte ancestry. Mol. Gen. Genet. 243 (1994) 249-252
62. Yoon H.S., Hackett J.D., Ciniglia C., Pinto G., and Bhattacharya D. A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 21 (2004) 809-818
63. Yoon H.S., Hackett J.D., Pinto G., and Bhattacharya D. The single, ancient origin of chromist plastids. Proc. Natl. Acad. Sci. USA 99 (2002) 15507-15512
64. Yoon H.S., Hackett J.D., Van Dolah F.M., Nosenko T., Lidie K.L., and Bhattacharya D. Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol. Biol. Evol. 22 (2005) 1299-1308
65. Yoon H.S., Müller K.M., Sheath R.G., Ott F.D., and Bhattacharya D. Defining the major lineages of red algae (Rhodophyta). J. Phycol. 42 (2006) 482-492
66. Zhang Z., Green B.R., and Cavalier-Smith T. Phylogeny of ultra-rapidly evolving dinoflagellate chloroplast genes: a possible common origin for sporozoan and dinoflagellate plastids. J. Mol. Evol. 51 (2000) 26-40