Diversity and evolutionary history of plastids and their hosts

American Journal of Botany

Volumn 91, Issue 10, 2004, Pages 1481-1493

  Keeling, Patrick J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Algae; Endosymbiosis; Phylogeny; Plastid; Tree of eukaryotes

Indexed keywords

ENDOSYMBIONT; EVOLUTION; PHYLOGENY; PLASTID;

ALGAE; ALVEOLATA; AMOEBA (GENUS); CHLORARACHNIOPHYCEAE; CHLOROPHYTA; CRYPTOPHYTA; DINOPHYCEAE; EUGLENA; EUGLENIDA; EUKARYOTA; GLAUCOCYSTOPHYCEAE; HAPTOPHYCEAE; PAULINELLA; RHODOPHYTA; STRAMENOPILES;

EID: 13244259056     PISSN: 00029122     EISSN: 00029122     Source Type: Journal    
DOI: 10.3732/ajb.91.10.1481     Document Type: Review

References (128)

1. ANDERSEN, R. A. 1991. The cytoskeleton of chromophyte algae. Protoplasma 164: 143-159.
2. ARCHIBALD, J. M., AND P. J. KEELING. 2002. Recycled plastids: a green movement in eukaryotic evolution. Trends in Genetics 18: 577-584.
3. ARCHIBALD, J. M., D. LONGET, J. PAWLOWSKI, AND P. J. KEELING. 2002. A novel polyubiquitin structure in Cercozoa and Foraminifera: evidence for a new eukaryotic supergroup. Molecular Biology and Evolution 20: 62-66.
4. ARCHIBALD, J. M., M. B. ROGERS, M. TOOP, K. ISHIDA, AND P. J. KEELING. 2003. Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proceedings of the National Academy of Sciences, USA 100: 7678-7683.
5. BACHVAROFF, T. R., G. T. CONCEPCION, C. R. RODGERS, E. M. HERMAN, AND C. F. DELWICHE. 2004. Dinoflagellate expressed sequence tags data indicate massive transfer of chloroplast genes to the nuclear genome. Protist 155: 65-78.
6. BALDAUF, S. L. 1999. A search for the origins of animals and fungi: comparing and combining molecular data. American Naturalist 154: S178-S188.
7. BALDAUF, S. L., AND J. D. PALMER. 1993. Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins. Proceedings of the National Academy of Sciences, USA 90: 11558-11562.
8. BALDAUF, S. L., A. J. ROGER, I. WENK-SIEFERT, AND W. F. DOOLITTLE. 2000. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290: 972-977.
9. BHATTACHARYA, D., T. HELMCHEN, C. BIBEAU, AND M. MELKONIAN. 1995. Comparison of nuclear-encoded small-subunit ribosomal RNAs reveal the evolutionary position of the Glaucocystophyta. Molecular Biology and Evolution 12: 415-420.
10. BHATTACHARYA, D., T. HELMCHEN, AND M. MELKONIAN. 1995. Molecular evolutionary analyses of nuclear-encoded small subunit ribosomal RNA identify an independent rhizopod lineage containing the Euglyphidae and the Chlorarachniophyta. Journal of Eukaryotic Microbiology 42: 64-68.
11. BHATTACHARYA, D., AND M. MELKONIAN. 1995. The phylogeny of plastids: a review based on comparisons of small-subunit ribosomal RNA coding regions. Journal of Phycology 31: 489-498.
12. BHATTACHARYA, D., AND H. A. SCHMIDT. 1997. Division Glaucocystophyta. In D. Bhattacharya [ed.], Origin of algae and their plastids, 139-148. Springer-Verlag, Wein, Austria.
13. BHATTACHARYA, D., AND K. WEBER. 1997. The actin gene of the glaucocystophyte Cyanophora paradoxa: analysis of the coding region and introns, and an actin phylogeny of eukaryotes. Current Genetics 31: 439-446.
14. BLANCHARD, J. L., AND J. S. HICKS. 1999. The non-photosynthetic plastid in malarial parasites and other apicomplexans is derived from outside the green plastid lineage. Journal of Eukaryotic Microbiology 46: 367-375.
15. BRUGEROLLE, G., AND F. J. R. TAYLOR. 1977. Taxonomy, cytology and evolution of the Mastigophora. In S. H. Hutner [ed.], Proceedings of the Fifth International Congress of Protozoology, 1977, 14-28. Pace University, New York, New York, USA.
16. BURGER, G., D. SAINT-LOUIS, M. W. GRAY, AND B. F. LANG. 1999. Complete sequence of the mitochondrial DNA of the red alga Porphyra purpurea. Cyanobacterial introns and shared ancestry of red and green algae. Plant Cell 11: 1675-1694.
17. CAI, X., A. L. FULLER, L. R. MCDOUGALD, AND G. ZHU. 2003. Apicoplast genome of the coccidian Eimeria tenella. Gene 321: 39-46.
18. CAVALIER-SMITH, T. 1981. Eukaryote kingdoms: seven or nine? Biosystems 14: 461-481.
19. CAVALIER-SMITH, T. 1982. The origins of plastids. Biological Journal of the Linaen Society 17: 289-306.
20. CAVALIER-SMITH, T. 1998. A revised six-kingdom system of life. Biological Reviews of the Cambridge Philosophical Society 73: 203-266.
21. CAVALIER-SMITH, T. 1999. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. Journal of Eukaryotic Microbiology 46: 347-366.
22. CAVALIER-SMITH, T. 2000. Membrane heredity and early chloroplast evolution. Trends in Plant Science 5: 174-182.
23. CAVALIER-SMITH, T., AND E. E. CHAO. 1997. Sarcomonad ribosomal RNA sequences, rhizopod phylogeny, and the origin of euglyphid amoebae. Archiv für Protistenkunde 147: 227-236.
24. CAVALIER-SMITH, T., AND E. E. CHAO. 2003. Phylogeny and classification of phylum Cercozoa (Protozoa). Protist 154: 341-358.
25. CHRISTEN, H. R. 1962. Neue und wenig bekannte Eugleninen und Volvocalen. Revue Algologique 4: 162-202.
26. DACKS, J. B., A. MARINETS, W. FORD DOOLITTLE, T. CAVALIER-SMITH, AND J. M. LOGSDON, JR. 2002. Analyses of RNA polymerase II genes from free-living protists: phylogeny, long branch attraction, and the eukaryotic big bang. Molecular Biology and Evolution 19: 830-840.
27. DAUGBJERG, N., AND R. A. ANDERSEN. 1997. Phylogenetic analyses of the rbcL sequences from haptophytes and heterokont algae suggest their chloroplasts are unrelated. Molecular Biology and Evolution 14: 1242-1251.
28. DEANE, J., D. R. A. HILL, S. J. BRETT, AND G. I. MCFADDEN. 1998. Hanusia phi gen. et sp. nov. (Cryptophyceae): characterization of 'Cryptomonas sp. Phi'. European Journal of Phycology 33: 149-154.
29. DELWICHE, C. F., M. KUHSEL, AND J. D. PALMER. 1995. Phylogenetic analysis of tufA sequences indicates a cyanobacterial origin of all plastids. Molecular Phylogenetics and Evolution 4: 110-128.
30. DODGE, J. D. 1969. Observatons on the fine structure of the eyespot and associated organelles in the dinoflagellate Glenodinium foliaceum. Journal of Cell Science 5: 479-493.
31. DODGE, J. D. 1971. A dinoflagellate with both a mesokaryotic and a eukayotic nucleus. I. Fine structure of the nuclei. Protoplasma 73: 145-157.
32. DOUGLAS, S., S. ZAUNER, M. FRAUNHOLZ, M. BEATON, S. PENNY, L. T. DENG, X. WU, M. REITH, T. CAVALIER-SMITH, AND U. G. MAIER. 2001. The highly reduced genome of an enslaved algal nucleus. Nature 410: 1091-1016.
33. DURNFORD, D. G., J. A. DEANE, S. TAN, G. I. MCFADDEN, E. GANTT, AND B. R. GREEN. 1999. A phylogenetic assessment of the eukaryotic lightharvesting antenna proteins, with implications for plastid evolution. Journal of Molecular Evolution 48: 59-68.
34. EMBLEY, T. M., AND R. P. HIRT. 1998. Early branching eukaryotes? Current Opinion in Genetics and Development 8: 624-629.
35. FAGAN, T., J. W. HASTINGS, AND D. MORSE. 1998. The phylogeny of glyceraldehyde-3-phosphate dehydrogenase indicates lateral gene transfer from cryptomonads to dinoflagellates. Journal of Molecular Evolution 47: 633-639.
36. FAST, N. M., J. C. KISSINGER, D. S. ROOS, AND P. J. KEELING. 2001. Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Molecular Biology and Evolution 18: 418-426.
37. FAST, N. M., L. XUE, S. BINGHAM, AND P. J. KEELING. 2002. Re-examining alveolate evolution using multiple protein molecular phylogenies. Journal of Eukaryotic Microbiology 49: 30-37.
38. FOTH, B. J., AND G. I. MCFADDEN. 2003. The apicoplast: a plastid in Plasmodium falciparum and other apicomplexan parasites. International Review of Cytology 224: 57-110.
39. FOTH, B. J., S. A. RALPH, C. J. TONKIN, N. S. STRUCK, M. FRAUNHOLZ, D. S. ROOS, A. F. COWMAN, AND G. I. MCFADDEN. 2003. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299: 705-708.
40. FRAUNHOLZ, M. J., J. WASTL, S. ZAUNER, S. A. RENSING, M. M. SCHERZINGER, AND U.-G. MAIER. 1997. The evolution of cryptophytes. Plant Systematics and Evolution (Supplement) 11: 163-174.
41. FUNES, S., E. DAVIDSON, A. REYES-PRIETO, S. MAGALLÖN, P. HERION, M. P. KING, AND D. GONZALEZ-HALPHEN. 2002. A green algal apicoplast ancestor. Science 298: 2155.
42. GARDNER, M. J., N. GOLDMAN, P. BARNETT, P. W. MOORE, K. RANGACHARI, M. STRATH, A. WHYTE, D. H. WILLIAMSON, AND R. J. WILSON. 1994. Phylogenetic analysis of the rpoB gene from the plastid-like DNA of Plasmodium falciparum. Molecular and Biochemical Parasitology 66: 221-231.
43. GARDNER, M. J., N. HALL, E. FUNG, O. WHITE, M. BERRIMAN, R. W. HYMAN, J. M. CARLTON, A. PAIN, K. E. NELSON, S. BOWMAN, I. T. PAULSEN, K. JAMES, J. A. EISEN, K. RUTHERFORD, S. L. SALZBERG, A. CRAIG, S. KYES, M. S. CHAN, V. NENE, S. J. SHALLOM, B. SUH, J. PETERSON, S. ANGIUOLI, M. PERTEA, J. ALLEN, J. SELENGUT, D. HAFT, M. W. MATHER, A. B. VAIDYA, D. M. MARTIN, A. H. FAIRLAMB, M. J. FRAUNHOLZ, D. S. ROOS, S. A. RALPH, G. I. MCFADDEN, L. M. CUMMINGS, G. M. SUBRAMANIAN, C. MUNGALL, J. C. VENTER, D. J. CARUCCI, S. L. HOFFMAN, C. NEWBOLD, R. W. DAVIS, C. M. FRASER, AND B. BARRELL. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
44. GRAY, M. W., AND W. F. DOOLITTLE. 1982. Has the endosymbiont hypothesis been proven? Microbiological Reviews 46: 1-42.
45. GREEN, B. R. 2004. The chloroplast genome of dinoflagellates - a reduced instruction set? Protist 155: 23-31.
46. GROSS, W., D. LENZE, U. NOWITZKI, J. WEISKE, AND C. SCHNARRENBERGER. 1999. Characterization, cloning, and evolutionary history of the chloroplast and cytosolic class I aldolases of the red alga Galdieria sulphuraria. Gene 230: 7-14.
47. GRZEBYK, D., O. SCHOFIELD, C. VETRIANI, AND P. G. FALKOWSKI. 2003. The mesozoic radiation of eukaryotic algae: the portable plastid hypothesis. Journal of Phycology 39: 259-267.
48. HACKETT, J. D., L. MARANDA, H. S. YOON, AND D. BHATTACHARYA. 2003. Phylogenetic evidence for the cryptophyte origin of the plastid of Dinophysis (Dinophysiales, Dinophyceae). Journal of Phycology 39: 440-448.
49. HACKETT, J. D., H. S. YOON, M. B. SOARES, M. F. BONALDO, T. L. CASAVANT, T. E. SCHEETZ, T. NOSENKO, AND D. BHATTACHARYA. 2004. Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Current Biology 14: 213-218.
50. HALLEGRAEFF, G. M., AND I. A. N. LUCAS. 1988. The marine dinoflagellate genus Dinophysis (Dinophyceae): photosynthetic, neritic and non-photosynthetic, oceanic species. Phycologia 27: 25-42.
51. HANNAERT, V., E. SAAVEDRA, F. DUFFIEUX, J.-P. SZIKORA, D. J. RIGDEN, P. A. M. MICHELS, AND F. R. OPPERDOES. 2003. Plant-like traits associated with metabolism of Trypanosoma parasites. Proceedings of the National Academy of Sciences, USA 100: 1067-1071.
52. HARPER, J. T., AND P. J. KEELING. 2003. Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Molecular Biology and Evolution 20: 1730-1735.
53. HARPER, J. T., AND P. J. KEELING. In press. On the monophyly of the chromalveolates using a six-protein phylogeny of eukaryotes. International Journal of Systematic and Evolutionary Microbiology.
54. HASEGAWA, M., T. HASHIMOTO, J. ADACHI, N. IWABE, AND T. MIYATA. 1993. Early branchings in the evolution of eukaryotes: ancient divergence of Entamoeba that lacks mitochondria revealed by protein sequence data. Journal of Molecular Evolution 36: 380-388.
55. HELMCHEN, T. A., D. BHATTACHARYA, AND M. MELKONIAN. 1995. Analyses of ribosomal RNA sequences from glaucocystophyte cyanelles provide new insights into the evolutionary relationships of plastids. Journal of Molecular Evolution 41: 203-210.
56. INAGAKI, Y., J. B. DACKS, W. F. DOOLITTLE, K. I. WATANABE, AND T. OHAMA. 2000. Evolutionary relationship between dinoflagellates bearing obligate diatom endosymbionts: insight into tertiary endosymbiosis. International Journal of Systematic and Evolutionary Microbiology 50: 2075-2081.
57. INAGAKI, Y., A. G. SIMPSON, J. B. DACKS, AND A. J. ROGER. In press. Phylogenetic artifacts can be caused by leucine, serine and arginine codon useage heterogeneity: dinoflagellate plastid origins as a case study. Systematic Biology.
58. ISHIDA, K., AND B. R. GREEN. 2002. Second- and third-hand chloroplasts in dinoflagellates: phylogeny of oxygen-evolving enhancer 1 (PsbO) protein reveals replacement of a nuclear-encoded plastid gene by that of a haptophyte tertiary endosymbiont. Proceedings of the National Academy of Sciences, USA 99: 9294-9299.
59. JARVIS, P., AND J. SOLL. 2001. Toc, Tic, and chloroplast protein import. Biochimica et Biophysica Acta 1541: 64-79.
60. JOHNSON, P. W., P. E. HARGRAVES, AND J. M. SIEBURTH. 1988. Ultrastructure and ecology of Calycomonas ovalis Wulff, 1919, (Chrysophyceae) and its redescription as a testate rhizopod, Paulinella ovalis n. comb. (Filosea: Euglyphina). Journal of Protozoology 35: 618-626.
61. KEELING, P. J. 2001. Foraminifera and Cercozoa are related in actin phylogeny: two orphans find a home? Molecular Biology and Evolution 18: 1551-1557.
62. KEELING, P. J., J. A. DEANE, C. HINK-SCHAUER, S. E. DOUGLAS, U. G. MAIER, AND G. I. MCFADDEN. 1999. The secondary endosymbiont of the cryptomonad Guillardia theta contains alpha-, beta-, and gammatubulin genes. Molecular Biology and Evolution 16: 1308-1313.
63. KEELING, P. J., J. A. DEANE, AND G. I. MCFADDEN. 1998. The phylogenetic position of alpha- and beta-tubulins from the Chlorarachnion host and Cercomonas (Cercozoa). Journal of Eukaryotic Microbiology 45: 561-570.
64. KEELING, P. J., AND W. F. DOOLITTLE. 1996. Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. Molecular Biology and Evolution 13: 1297-1305.
65. KEELING, P. J., AND J. D. PALMER. 2001. Lateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase. Proceedings of the National Academy of Sciences, USA 98: 10745-10750.
66. KIES, L. 1974. Elektronenmikroskopische Untersuchungen an Paulinella chromatophora Lauterborn, einer Thekamöbe mit blau-grünen Endosymbionten (Cyanellen). Protoplasma 80: 69-89.
67. KIES, L., AND B. P. KREMER. 1979. Function of cyanelles in the thecamoeba Paulinella chromatophora. Naturewissenschaften 66: 578-579.
68. KITE, G. C., AND J. D. DODGE. 1988. Cell and chloroplast ultrastructure in Gyrodinium aureolum and Gymnodinium galatheanum. Two marine dinoflagellates containing an unusual carotenoid. Sarsia 73: 131-138.
69. KIVIC, P. A., AND P. L. WALNE. 1984. An evaluation of a possible phylogenetic relationship between the Euglenophyta and Kinetoplastida. Origins of Life 13: 269-288.
70. KÖHLER, S., C. F. DELWICHE, P. W. DENNY, L. G. TILNEY, P. WEBSTER, R. J. M. WILSON, J. D. PALMER, AND D. S. ROOS. 1997. A plastid of probable green algal origin in apicomplexan parasites. Science 275: 1485-1489.
71. KOWALLIK, K. V. 1997. Origin and evolution of chloroplasts: current status and future perspectives. In H. E. Schenk, R. G. Herrmann, K. W. Jeon, N. E. Müller, and W. Schwemmler [eds.], Eukaryotism and symbiosis: intertaxonic combination versus symbiotic adaptation, 3-23. Springer, Berlin, Germany.
72. LEANDER, B. S., R. P. WITEK, AND M. A. FARMER. 2001. Trends in the evolution of the euglenid pellicle. Evolution 55: 2215-2235.
73. LEEDALE, G. F. 1967. Euglenoid flagellates. Prentice-Hall, Englewood Cliffs, New Jersey, USA.
74. LEEDALE, G. F., AND K. VICKERMAN. 2000. Phylum Euglenozoa. In J. J. Lee, G. F. Leedale, and P. Bradbury [eds.], An illustrated guide to the protozoa, 2nd ed., 1135-1185. Society of Protozoologists, Lawrence, Kansas, USA.
75. LIAUD, M. F., C. LICHTLE, K. APT, W. MARTIN, AND R. CERFF. 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 glycolytic pathway. Molecular Biology and Evolution 17: 213-223.
76. LONGET, D., J. M. ARCHIBALD, P. J. KEELING, AND J. PAWLOWSKI. 2003. Foraminifera and Cercozoa share a common origin according to RNA polymerase II phylogenies. International Journal of Systematic and Evolutionary Microbiology 53: 1735-1739.
77. MARTIN, W., T. RUJAN, E. RICHLY, A. HANSEN, S. CORNELSEN, T. LINS, D. LEISTER, B. STOEBE, M. HASEGAWA, AND D. PENNY. 2002. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proceedings of the National Academy of Sciences, USA 99: 12246-12251.
78. MARTIN, W., B. STOEBE, V. GOREMYKIN, S. HANSMANN, M. HASEGAWA, AND K. V. KOWALLIK. 1998. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393: 162-165.
79. MCFADDEN, G. I. 1999. Plastids and protein targeting. Journal of Eukaryotic Microbiology 46: 339-346.
80. MCFADDEN, G. I., P. R. GILSON, S. E. DOUGLAS, T. CAVALIER-SMITH, C. J. HOFMANN, AND U. G. MAIER. 1997a. Bonsai genomics: sequencing the smallest eukaryotic genomes. Trends in Genetics 13: 46-49.
81. MCFADDEN, G. I., P. R. GILSON, AND C. J. B. HOFMANN. 1997b. Division Chlorarachniophyta. Springer-Verlag, New York, New York, USA.
82. MCFADDEN, G. I., P. R. GILSON, AND R. F. WALLER. 1995. Molecular phylogeny of chlorarachniophytes based on plastid rRNA and rbcL sequences. Archiv für Protistenkunde 145: 231-239.
83. MCFADDEN, G. I., M. REITH, J. MUNHOLLAND, AND N. LANG-UNNASCH. 1996. Plastids in human parasites. Nature 381: 482.
84. MCFADDEN, G. I., AND R. F. WALLER. 1997. Plastids in parasites of humans. Bioessays 19: 1033-1040.
85. MEDLIN, L. K., A. COOPER, C. HILL, S. WRIEDEN, AND U. WELLBROCK. 1995. Phylogenetic position of the Chromista plastids based on small subunit rRNA coding regions. Current Genetics 28: 560-565.
86. MOREIRA, D., H. LE GUYADER, AND H. PHILLIPPE. 2000. The origin of red algae and the evolution of chloroplasts. Nature 405: 69-72.
87. MULLER, K. M., M. C. OLIVEIRA, R. G. SHEATH, AND D. BHATTACHARYA. 2001. Ribosomal DNA phylogeny of the Bangiophycidae (Rhodophyta) and the origin of secondary plastids. American Journal of Botany 88: 1390-1400.
88. NASSOURY, N., M. CAPPADOCIA, AND D. MORSE. 2003. Plastid ultrastructure defines the protein import pathway in dinoflagellates. Journal of Cell Science 116: 2867-2874.
89. NICKOL, A. A., N. E. MULLER, U. BAUSENWEIN, M. G. BAYER, T. L. MAIER, AND H. E. SCHENK. 2000. Cyanophora paradoxa: nucleotide sequence and phylogeny of the nucleus encoded muroplast fructose-1,6-bisphosphate aldolase. Zeitschrift für Naturforschung 55: 991-1003.
90. OLIVEIRA, M. C., AND D. BHATTACHARYA. 2000. Phylogeny of the Bangiophycidae (Rhodophyta) and the secondary endosymbiotic origin of algal plastids. American Journal of Botany 87: 482-492.
91. PALMER, J. D. 2003. The symbiotic birth and spread of plastids: how many times and whodunit? Journal of Phycology 39: 1-9.
92. PATRON, N. J., M. B. ROGERS, AND P. J. KEELING. In press. Gene replacement of fructose-1,6-bisphosphate aldolase (FBA) supports a single photosynthetic ancestor of chromalveolates. Eukaryotic Cell.
93. PHILIPPE, H., P. LOPEZ, H. BRINKMANN, K. BUDIN, A. GERMOT, J. LAURENT, D. MOREIRA, M. MULLER, AND H. LE GUYADER. 2000. Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proceedings of the Royal Society of London, B, Biological Sciences 267: 1213-1221.
94. RALPH, S. A., G. G. VAN DOOREN, R. F. WALLER, M. J. CRAWFORD, M. FRAUNHOLZ, B. J. FOTH, D. S. ROOS, AND G. I. MCFADDEN. 2004. The relict plastid of the malaria parasite Plasmodium falciparum: metabolic pathways and function. Nature Reviews Microbiology 2: 203-216.
95. ROGERS, M. B., AND P. J. KEELING. 2003. Lateral gene transfer and re-compartmentalisation of Calvin cycle enzymes in plants and algae. Journal of Molecular Evolution 58: 367-375.
96. SALDARRIAGA, J. F., M. L. MCEWAN, N. M. FAST, F. J. R. TAYLOR, AND P. J. KEELING. 2003. Multiple protein phylogenies show that Oxyhrris marina and Perkinsus marinus are early branches of the dinoflagellate lineage. International Journal of Systematic and Evolutionary Microbiology 53: 355-365.
97. SALDARRIAGA, J. F., F. J. R. TAYLOR, P. J. KEELING, AND T. CAVALIER-SMITH. 2001. Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. Journal of Molecular Evolution 53: 204-213.
98. SCHNEPF, E., AND M. ELBRÄCHTER. 1988. Cryptophycean-like double membrane-bound chloroplast in the dinoflagellate, Dinophysis Ehrenb.: evolutionary, phylogenetic and toxicological implications. Botanica Acta 101: 196-203.
99. SIMPSON, A. G. 2003. Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). International Journal of Systematic and Evolutionary Microbiology 53: 1759-1777.
100. SIMPSON, A. G., AND D. J. PATTERSON. 2001. On core jakobids and excavate taxa: the ultrastructure of Jakoba incarcerata. Journal of Eukaryotic Microbiology 48: 480-492.
101. SOGIN, M. L. 1991. Early evolution and the origin of eukaryotes. Current Opinion in Genetics & Development 1: 457-463.
102. SOGIN, M. L., H. J. ELWOOD, AND J. H. GUNDERSON. 1986. Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proceedings of the National Academy of Sciences, USA 83: 1383-1387.
103. STECHMANN, A., AND T. CAVALIER-SMITH. 2002. Rooting the eukaryote tree by using a derived gene fusion. Science 297: 89-91.
104. STEIDINGER, K. A., E. W. TRUBY, AND C. J. DAWES. 1978. Ultrastructure of the red tide dinoflagellate Gymnodinium breve, part 1. General description. Journal of Phycology 14: 72-79.
105. STEINER, J. M., AND W. LOFFELHARDT. 2002. Protein import into cyanelles. Trends in Plant Sciences 7: 72-77.
106. STILLER, J. W., AND B. D. HALL. 1997. The origin of red algae: implications for plastid evolution. Proceedings of the National Academy of Sciences, USA 94: 4520-4525.
107. SULLI, C., Z. FANG, U. MUCHHAL, AND S. D. SCHWARTZBACH. 1999. Topology of Euglena chloroplast protein precursors within endoplasmic reticulum to Golgi to chloroplast transport vesicles. Journal of Biological Chemistry 274: 457-463.
108. TAKISHITA, K., K. KOIKE, T. MARUYAMA, AND T. OGATA. 2002. Molecular evidence for plastid robbery (kleptoplastidy) in Dinophysis, a dinoflagellate causing diarrhetic shellfish poisoning. Protist 153: 293-302.
109. TAYLOR, F. J. 1978. Problems in the development of an explicit hypothetical phylogeny of the lower eukaryotes. Biosystems 10: 67-89.
110. TAYLOR, F. J. R. E. 1987. The biology of dinoflagellates. Blackwell Scientific Publications, Oxford, UK.
111. TENGS, T., O. J. DAHLBERG, K. SHALCHIAN-TABRIZI, D. KLAVENESS, K. RUDI, C. F. DELWICHE, AND K. S. JAKOBSEN. 2000. Phylogenetic analyses indicate that the 199 hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Molecular Biology and Evolution 17: 718-729.
112. TOMAS, R. N., E. R. COX, AND K. A. STEIDINGER. 1973. Peridinium balticum (Levander) Lemmermann, an unusual dinoflagellate with a mesokaryotic and an eukaryotic nucleus. Journal of Phycology 9: 91-98.
113. TURMEL, M., C. OTIS, AND C. LEMIEUX. 1999. The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architecture of ancestral chloroplast genomes. Proceedings of the National Academy of Sciences, USA 96: 10248-10253.
114. TURNER, S. 1997. Molecular systematics of oxygenic photosynthetic bacteria. Plant Systematics and Evolution (Supplement) 11: 13-52.
115. TURNER, S., K. M. PRYER, V. P. MIAO, AND J. D. PALMER. 1999. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. Journal of Eukaryotic Microbiology 46: 327-338.
116. VALENTIN, K., AND K. ZETSCHE. 1990. Nucleotide sequence of the gene for the large subunit of Rubisco from Cyanophora paradoxa - phylogenetic implications. Current Genetics 18: 199-202.
117. VAN DE PEER, Y., AND R. DE WACHTER. 1997. Evolutionary relationships among eukaryotic crown taxa taking into account site-to-site variation in 18S rRNA. Journal of Molecular Evolution 45: 619-630.
118. VAN DE PEER, Y., G. VAN DER AUWERA, AND R. DE WACHTER. 1996. The evolution of stramenopiles and alveolates as derived by "substitution rate calibration" of small ribosomal subunit RNA. Journal of Molecular Evolution 42: 201-210.
119. WALLER, R. F., P. J. KEELING, G. G. VAN DOOREN, AND G. I. MCFADDEN. 2003. Comment on "A green algal apicoplast ancestor". Science 301: 49.
120. WATANABE, M. M., S. SUDA, I. INOUYE, I. SAWAGUCHI, AND M. CHIHARA. 1990. Lepidodinium viride gen. et sp. nov. (Gymnodiniales, Dinophyta), a green dinoflagellate with a chlorophyll a- and b-containing endosymbiont. Journal of Phycology 26: 741-751.
121. WATANABE, M. M., Y. TAKEDA, T. SASA, S. SUDA, T. SAWAGUCHI, AND M. CHIHARA. 1987. A green dinoflagellate with chlorophylls a and b: morphology, fine structure of the chloroplast and chlorophyll composition. Journal of Phycology 23: 382-389.
122. WILLIAMS, B. A. P., AND P. J. KEELING. 2003. Cryptic organelles in parasitic protists and fungi. Advances in Parasitology 54: 9-67.
123. WILSON, R. J. 2002. Progress with parasite plastids. Journal of Molecular Biology 319: 257-274.
124. WILSON, R. J. M. I., P. W. DENNY, D. J. PREISER, K. RANGACHARI, K. ROBERTS, A. ROY, A. WHYTE, M. STRATH, D. J. MOORE, P. W. MOORE, AND D. H. WILLIAMSON. 1996. Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. Journal of Molecular Biology 261: 155-172.
125. YOON, H. S., J. D. HACKETT, AND D. BHATTACHARYA. 2002. A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proceedings of the National Academy of Sciences, USA 99: 11724-11729.
126. YOON, H. S., J. D. HACKETT, G. PINTO, AND D. BHATTACHARYA. 2002. A single, ancient origin of the plastid in the Chromista. Proceedings of the National Academy of Sciences, USA 99: 15507-15512.
127. ZHANG, Z., B. R. GREEN, AND T. CAVALIER-SMITH. 2000. Phylogeny of ultrarapidly evolving dinoflagellate chloroplast genes: a possible common origin for sporozoan and dinoflagellate plastids. Journal of Molecular Evolution 51: 26-40.
128. ZHANG, Z., B. R. GREEN, AND T. CAVALIER-SMITH. 1999. Single gene circles in dinoflagellate chloroplast genomes. Nature 400: 155-159.