Dinoflagellates: A remarkable evolutionary experiment

American Journal of Botany

Volumn 91, Issue 10, 2004, Pages 1523-1534

  Hackett, Jeremiah D ^a   Anderson, Donald M ^b   Erdner, Deana L ^b   Bhattacharya, Debashish ^a  

^a UNIVERSITY OF IOWA   (United States)

^b WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

Author keywords

Dinoflagellate; Endosymbiosis; Evolution; Harmful algal blooms

Indexed keywords

DINOFLAGELLATE; ENDOSYMBIONT; EVOLUTION; FOSSIL RECORD; PHYLOGENY;

ALGAE; ANTHOZOA; DINOPHYCEAE; EUKARYOTA;

EID: 17644425978     PISSN: 00029122     EISSN: 00029122     Source Type: Journal    
DOI: 10.3732/ajb.91.10.1523     Document Type: Review

References (142)

1. ALLEN, J. F. 2003. The function of genomes in bioenergetic organelles. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 358: 19-37.
2. ALLEN, J. F., AND J. A. RAVEN. 1996. Free-radical-induced mutation vs redox regulation: costs and benefits of genes in organelles. Journal of Molecular Evolution 42: 482-492.
3. ALLEN, J. R., T. M. ROBERTS, A. R. LOEBLICH III, AND L. C. KLOTZ. 1975. Characterization of the DNA from the dinoflagellate Crypthecodinium cohnii and implications for nuclear organization. Cell 6: 161-169.
4. ANDERSON, D. M., AND K. D. STOLZENBACH. 1985. Selective retention of two dinoflagellates in a well-mixed estuarine embayment: the importance of diel vertical migration and surface avoidance. Marine Ecology Progress Series 25: 39-50.
5. ANDERSON, D. M., AND P. S. LOBEL. 1987. The continuing enigma of ciguatera. Biological Bulletin 172: 89-107.
6. ANDERSON, D. M., A. GRABHER, AND M. HERZOG. 1992. Separation of coding sequences from structural DNA in the dinoflagellate Crypthecodinium cohnii. Molecular Marine Biology and Biotechnology 1: 89-96.
7. 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.
8. BACHVAROFF, T. R., G. T. CONCEPCION, C. R. ROGERS, E. M. HERMAN, AND C. F. DELWICHE. 2004. Dinoflagellate expressed sequence tag data indicate massive transfer of chloroplast genes to the nuclear genome. Protist 155: 65-78.
9. BALDAUF, S. L., A. J. ROGER, I. WENK-SIEFERT, AND W. F. DOOLITTLE. 2000. A kingdom level phylogeny based on combined protein data. Science 290: 972-977.
10. BANASZAK, A., R. IGLESIAS-PRIETO, AND R. K. TRENCH. 1993. Scrippsiella velellae sp. nov. (peridiniales) and Gloeodinium viscum sp. nov. (Phytodiniales), dinoflagellate symbionts of two hydrozoans (Cnidaria). Journal of Phycology 29: 517-528.
11. BARBROOK, A. C., AND C. J. HOWE. 2000. Minicircular plastid DNA in the dinoflagellate Amphidinium operculatum. Molecular and General Genetics 263: 152-158.
12. BEAM, J., AND M. HIMES. 1984. Dinoflagellate genetics. In D. L. Spector [ed.], Dinoflagellates, 263-298. Academic Press, Inc., Orlando, Florida, USA.
13. BHATTACHARYA, D., AND L. MEDLIN. 1995. The phylogeny of plastids: a review based on comparisons of small-subunit ribosomal RNA coding regions. Journal of Phycology 31: 489-498.
14. BHATTACHARYA, D., H. S. YOON, AND J. D. HACKETT. 2004. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 26: 50-60.
15. BURKHOLDER, J. M., H. B. GLASGOW, JR., AND A. J. LEWITUS. 1998. Physiological ecology of Pfiesteria piscicida with general comments on "ambush-predator" dinoflagellates. In D. M. Anderson, A. D. Cembella, and G. M. Hallegraeff [eds.], Physiological ecology of harmful algal blooms, 175-191. Springer-Verlag, Berlin, Germany.
16. BUSKEY, E. J., AND E. SWIFT. 1983. Behavioral responses of the coastal copepod Acartia hudsonica (Pinhey) to simulated dinoflagellate bioluminescence. Journal of Experimental Marine Biology and Ecology 72: 43-58.
17. CAVALIER-SMITH, T. 1991. Cell diversification in heterotrophic flagellates. In D. J. Patterson and J. Larsen [eds.], The biology of free-living heterotrophic flagellates, 113-131. Clarendon Press, Oxford, UK.
18. 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.
19. CHESNICK, J. M., C. W. MORDEN, AND A. M. SCHMIEG. 1996. Identity of the endosymbiont of Peridinium foliaceum (Pyrrophyta): analysis of the rbcLS operon. Journal of Phycology 32: 850-857.
20. CHESNICK, J. M., W. H. KOOISTRA, U. WELLBROCK, AND L. K. MEDLIN. 1997. Ribosomal RNA analysis indicates a benthic pennate diatom ancestry for the endosymbionts of the dinoflagellates Peridinium foliaceum and Peridinium balticum (Pyrrhophyta). Journal of Eukaryotic Microbiology 44: 314-320.
21. CULLEN, J. J., AND J. G. MACINTYRE. 1998. Behavior, physiology and the niche of depth-regulating phytoplankton. In D. M. Anderson, A. D. Cembella, and G. M. Hallegraeff [eds.], Physiological ecology of harmful algal blooms, 559-580. Springer-Verlag, Berlin, Germany.
22. DAUGBJERG, N., G. HANSEN, J. LARSEN, AND Ø. MOESTRUP. 2000. Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia 39: 302-317.
23. DAVIES, W., K. S. JAKOBSEN, AND O. NORDBY. 1988. Characterization of DNA from the dinoflagellate Woloszynskia bostoniensis. Journal of Protozoolology 35: 418-422.
24. DODGE, J. D. 1965. Chromosome structure in the dinoflagellates and the problem of mesokaryotic cells. Excerpta Medica, International Congress Series 91: 339-345.
25. DODGE, J. D. 1966. The Dinophyceae. In M. B. E. Godward [ed.], The chromosomes of the algae, 96-115. St. Martin's Press, New York, New York, USA.
26. 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: 1091-1096.
27. 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.
28. EDQVIST, J., G. BURGER, AND M. W. GRAY. 2000. Expression of mitochondrial protein-coding genes in Tetrahymena pyriformis. Journal of Molecular Biology 297: 381-393.
29. ELLEN, R., R. NISBET, V. LILA KOUMANDOU, A. C. BARBROOK, AND C. J. HOWE. 2004. Novel plastid gene minicircles in the dinoflagellate Amphidinium operculatum. Gene 331: 141-147.
30. FAGAN, T. F., D. MORSE, AND J. W. HASTINGS. 1999. Circadian synthesis of a nuclear-encoded chloroplast glyceraldehyde-3-phosphate dehydrogenase in the dinoflagellate Gonyaulax polyedra is translationally controlled. Biochemistry 38: 7689-7695.
31. FAST, N. M., J. C. KISSINGER, D. S. ROOS, AND P. J. KEELING. 2001. Nuclearencoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Molecular Biology and Evolution 18: 418-426.
32. 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.
33. FENSOME, R. A., F. J. R. TAYLOR, G. NORRIS, W. A. S. SARJEANT, D. I. WHARTON, AND G. L. WILLIAMS. 1993. A classification of living and fossil dinoflagellates. Micropaleontology Special Publication 7: 1-351.
34. FENSOME, R. A., J. F. SALDARRIAGA, AND F. J. R. TAYLOR. 1999. Dinoflagellate phylogeny revisited: reconciling morphological and molecular based phylogenies. Grana 38: 66-80.
35. FLANAGAN, A. F., K. R. CALLANAN, J. DONLON, R. PALMER, A. FORDE, AND M. KANE. 2001. A cytotoxicity assay for the detection and differentiation of two families of shellfish toxins. Toxicon 39: 1021-1027.
36. GAINES, G., AND M. ELBRACHTER. 1987. Heterotrophic nutrition. In F. J. R. Taylor [ed.], The biology of dinoflagellates, 224-267. Blackwell, Oxford, UK.
37. GAJADHAR, A. A., W. C. MARQUARDT, R. HALL, J. GUNDERSON, E. V. ARIZTIA-CARMONA, AND M. L. SOGIN. 1991. Ribosomal RNA sequences of Sarcocystis muris, Theileria annulata and Crypthecodinium cohnii reveal evolutionary relationships among apicomplexans, dinoflagellates, and ciliates. Molecular and Biochemical Parasitology 45: 147-154.
38. GALLACHER, S., K. J. FLYNN, J. M. FRANCO, E. E. BRUEGGEMANN, AND H. B. HINES. 1997. Evidence for production of paralytic shellfish toxins by bacteria associated with Alexandrium spp. (Dinophyta) in culture. Applied Environmental Microbiology 63: 239-245.
39. GETZENBERG, M. L., K. J. PIENTA, W. S. WARD, AND D. S. COFFEY. 1991. Nuclear structure and the three dimensional organization of DNA. Journal of Cellular Biochemistry 47: 289-299.
40. GRAHAM, L., AND L. W. WILCOX. 2000. Algae. Prentice-Hall, Upper Saddle River, New Jersey, USA.
41. GRAY, M. W. 2003. Diversity and evolution of mitochondrial RNA editing systems. IUBMB Life 55: 227-233.
42. GUILLOU, L., E. NÉZAN, V. CUEFF, E. ERARD-LE DENN, M.-A. CAMBON-BONAVITA, P. GENTIEN, AND G. BARBIER. 2002. Genetic diversity and molecular detection of three toxic dinoflagellate genera (Alexandrium, Dinophysis, and Karenia) from French coasts. Protist 153: 223-238.
43. GUNDERSON, J. H., S. H. GOSS, AND D. W. COATS. 1999. The phylogenetic position of Amoebophyra sp. from Gymnodinium sanguineum. Journal of Eukaryotic Microbiology 46: 195-197.
44. 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.
45. HACKETT, J. D., H. S. YOON, M. B. SOARES, M. F. BONALDO, T. 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.
46. HAGOPIAN, J. C., M. REIS, J. P. KITAJIMA, D. BHATTACHARYA, AND M. C. DE OLIVEIRA. In press. Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui: insights on the evolution of rhodoplasts and their relationship to other plastids. Journal of Molecular Evolution.
47. HALLEGRAEFF, G. M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32: 79-99.
48. HARPER, J. T., AND P. J. KEELING. 2003. Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromist and alveolate plastids. Molecular Biology and Evolution 20: 1730-1735.
49. HILLER, R. G. 2001. 'Empty' minicircles and petB/atpA and psbD/psbE (cytb559 a) genes in tandem in Amphidinium carterae plastid DNA. FEBS Letters 505: 449-452.
50. HINNEBUSCH, A. G., L. C. KLOTZ, E. IMMERGUT, AND A. R. LOEBLICH III. 1980. Deoxyribonucleic acid sequence organization in the genome of the dinoflagellate Crypthecodinium cohnii. Biochemistry 19: 1744-1755.
51. HOLD, G. L., E. A. SMITH, M. S. RAPPE, E. W. MAAS, E. R. B. MOORE, C. STROEMPL, J. R. STEPHEN, J. I. PROSSER, T. H. BIRKBECK, AND S. GALLACHER. 2001. Characterisation of bacterial communities associated with toxic and non-toxic dinoflagellates: Alexandrium spp. and Scrippsiella trochoidea. FEMS Microbiology Ecology 37: 161-173.
52. HOWE, C. J., A. C. BARBROOK, V. L. KOUMANDOU, R. E. NISBET, H. A. SYMINGTON, AND T. F. WIGHTMAN. 2003. Evolution of the chloroplast genome. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 358: 99-106.
53. 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 usage heterogeneity: dinoflagellate plastid origins as a case study. Systematic Biology.
54. 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.
55. ITO, E., M. SATAKE, K. OFUJI, M. HIGASHI, K. HARIGAYA, T. MCMAHON, AND T. YASUMOTO. 2002. Chronic effects in mice caused by oral administration of sublethal doses of azaspiracid, a new marine toxin isolated from mussels. Toxicon 40: 193-203.
56. JACOBSON, D. M. 1987. The ecology and feeding biology of thecate heterotrophic dinoflagellates. Ph.D. dissertation, Woods Hole Oceanographic Institution/Massachusetts Institute of Technology Joint Program in Oceanography and Oceanographic Engineering, Woods Hole, Massachusetts, USA.
57. JACOBSON, D. M., AND D. M. ANDERSON. 1992. Ultrastructure of the feeding apparatus and myonemal system of the heterotrophic dinoflagellate Protoperidinium spinulosum. Journal of Phycology 28: 69-82.
58. JAMES, K. J., C. MORONEY, C. RODEN, M. SATAKE, T. YASUMOTO, M. LEHANE, AND A. FUREY. 2003. Ubiquitous 'benign' alga emerges as the cause of shellfish contamination responsible for the human toxic syndrome, azaspiracid poisoning. Toxicon 41: 145-151.
59. JANSON, S., AND E. GRANÉLI. 2003. Genetic analysis of the psbA gene from single cells indicates a cryptomonad origin of the plastid in Dinophysis (Dinophyceae). Phycologia 42: 473-477.
60. KELLY, M. G., AND P. TETT. 1978. Bioluminescence in the ocean. In P. J. Herring [ed.], Bioluminescence in action, 399-417. Academic Press, London, UK.
61. KODAMA, M., T. OGATA, AND S. SATO. 1988. Saxitoxin-producing bacterium isolated from Protogonyaulax tamarensis. In T. Okaichi, D. M. Anderson, and T. Nemoto [eds.], Red tides: biology, environmental science and toxicology, 363-366. Elsevier, New York, New York, USA.
62. LAATSCH, T., S. ZAUNER, B. STOEBE-MAIER, K. V. KOWALLIK, AND U. G. MAIER. 2004. Plastid-derived single gene minicircles of the dinoflagellate Ceratium horridum are localized in the nucleus. Molecular Biology and Evolution: Advance Access published on 19 March 2004, DOI: 10.1093/molbev/msh127.
63. LE, Q. H., P. MARKOVIC, J. W. HASTINGS, R. V. M. JOVINE, AND D. MORSE. 1997. Structure and organization of the peridinin-chlorophyll a-binding protein gene in Gonyaulax polyedra. Molecular and General Genetics 255: 595-604.
64. LEE, D.-H., M. MITTAG, S. SCZEKAN, D. MORSE, AND J. W. HASTINGS. 1993. Molecular cloning and genomic organization of a gene for luciferin-binding protein from the dinoflagellate Gonyaulax polyedra. Journal of Biological Chemistry 268: 8842-8850.
65. LEGGAT, W., M. R. BADGER, AND D. YELLOWLEES. 1999. Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiology 121: 1247-1256.
66. LEHANE, L., AND R. J. LEWIS. 2000. Ciguatera: recent advances but the risk remains. International Journal of Food Microbiology 61: 91-125.
67. LEVASSEUR, M., P. MONFORT, G. J. DOUCETTE, AND S. MICHAUD. 1996. Preliminary study of bacteria as PSP producers in the Gulf of St. Lawrence, Canada. In T. Yasumoto, Y. Oshima, and Y. Fukuyo [eds.], Harmful and toxic algal blooms, 363-366. Intergovernmental Oceanographic Commission of UNESCO, Paris, France.
68. LI, L., AND J. W. HASTINGS. 1998. The structure and organization of the luciferase gene in the photosynthetic dinoflagellate Gonyaulax polyedra. Plant Molecular Biology 36: 275-284.
69. LILLY, E. L. 2003. Phylogeny and biogeography of the toxic dinoflagellate Alexandrium. Ph.D. dissertation, Massachusetts Institute of Technology and Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, USA.
70. LIN, S., H. ZHANG, D. F. SPENCER, J. E. NORMAN, AND M. W. GRAY. 2002. Widespread and extensive editing of mitochondrial mRNAs in dinoflagellates. Journal of Molecular Biology 320: 727-739.
71. LOEBLICH, A. R. 1976. Dinoflagellate evolution: speculation and evidence. Journal of Protozoolology 23: 13-28.
72. LÓPEZ-GARCÍA, P., F. RODRÍGUEZ-VALERA, C. PEDRÓS-ALIÓ, AND D. MOREIRA. 2001. Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409: 603-607.
73. MARSHALL, A. 1996. Calcification in hermatypic and ahermatypic corals. Science 271: 1788-1792.
74. MARTIN, W., AND R. G. HERRMANN. 1998. Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiology 118: 9-17.
75. MCFADDEN, G. I. 1999. Plastids and protein targeting. Journal of Eukaryotic Microbiology 46: 339-346.
76. MCNALLY, K. L., N. S. GOVIND, P. E. THOMÉ, AND R. K. TRENCH. 1994. Small-subunit ribosomal DNA sequence analysis and a reconstruction of the inferred phylogeny among symbiotic dinoflagellates (Pyrrophyta). Journal of Phycology 30: 316-329.
77. MOLDOWAN, J. M., J. DAHL, S. R. JACOBSON, B. J. HUIZINGA, F. J. FAGO, R. SHETTY, D. S. WATT, AND K. E. PETERS. 1996. Chemostratographic reconstruction of biofacies: molecular evidence linking cyst-forming dinoflagellates with pre-Triassic ancestors. Geology 24: 159-162.
78. MOLDOWAN, J. M., AND N. M. TALYZINIA. 1998. Biogeochemical evidence for dinoflagellate ancestors in the early Cambrian. Science 281: 1168-1170.
79. MOON-VAN DER STAAY, S. Y., R. DE WACHTER, AND D. VAULOT. 2001. Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409: 607-610.
80. MORDEN, C. W., AND A. R. SHERWOOD. 2002. Continued evolutionary surprises among dinoflagellates. Proceedings of the National Academy of Sciences, USA 99: 11558-11560.
81. MORSE, D., P. M. MILOS, E. ROUX, AND J. W. HASTINGS. 1989. Circadian regulation of bioluminescence in Gonyaulax involves translational control. Proceedings of the National Academy of Sciences, USA 86: 172-176.
82. MORSE, D., P. SALOIS, P. MARKOVIC, AND J. W. HASTINGS. 1995. A nuclearencoded Form II RuBisCO in dinoflagellates. Science 268: 1622-1624.
83. NASSOURY, N., M. CAPPADOCIA, AND D. MORSE. 2003. Plastid ultrastructure defines the protein import pathway in dinoflagellates. Journal of Cell Science 116: 2867-2874.
84. NOZAKI, H., M. MATSUZAKI, M. TAKAHARA, O. MISUMI, H. KUROIWA, M. HASEGAWA, T. SHIN-I, Y. KOHARA, N. OGASAWARA, AND T. KUROIWA. 2003. The phylogenetic position of red algae revealed by multiple nuclear genes from mitochondria-containing eukaryotes and an alternative hypothesis on the origin of plastids. Journal of Molecular Evolution 56: 485-497.
85. OAKLEY, B., AND J. D. DODGE. 1974. Kinetochores associated with the nuclear envelope in the mitosis of a dinoflagellate. Journal of Cell Biology 63: 322-325.
86. OKAMOTO, O. K., D. L. ROBERTSON, T. F. FAGAN, J. W. HASTINGS, AND P. COLEPICOLO. 2001. Different regulatory mechanisms modulate the expression of a dinoflagellate iron-superoxide dismutase. Journal of Biological Chemistry 276: 19989-19993.
87. OKAMOTO, O. K., AND J. W. HASTINGS. 2003. Genome wide analysis of redox-regulated genes in a dinoflagellate. Gene 321: 73-81.
88. O'SHEA, T. J., G. B. RATHBUN, R. K. BONDE, C. D. BUERGELT, AND D. K. ODELL. 1991. An epizootic of Florida manatees associated with a dinoflagellate bloom. Marine Mammal Science 7: 165-179.
89. OSHIMA, Y., H. ITAKURA, K.-C. LEE, T. YASUMOTO, S. BLACKBURN, AND G. HALLEGRAEFF. 1993. Toxin production by the dinoflagellate Gymnodinium catenatum. In T. J. Smayda and Y. Shimizu [eds.], Toxic phytoplankton blooms in the sea, 907-912. Elsevier, New York, New York, USA.
90. PALMER, J. D. 1995. Rubisco rules fall; gene transfer triumphs. Bioessays 17: 1005-1008.
91. PARACER, S., AND V. AHMADJIAN. 2000. Symbiosis: an introduction to biological associations. Oxford University Press, New York, New York, USA.
92. PEREIRA, P., H. ONODERA, D. ANDRINOLO, S. FRANCA, F. ARAUJO, N. LAGOS, AND Y. OSHIMA. 2000. Paralytic shellfish toxins in the freshwater cyanobacterium Aphanizomenon flosaquae, isolated from Montargil reservoir, Portugal. Toxicon 38: 1689-1702.
93. POMATI, F., S. SACCHI, C. ROSSETTI, S. GIOVANNARDI, H. ONODERA, Y. OSHIMA, AND B. A. NEILAN. 2000. The freshwater cyanobacterium Planktothrix sp. FP1: molecular identification and detection of paralytic shell-fish poisoning toxins. Journal of Phycology 36: 553-562.
94. RAE, P. M. M. 1976. Hydroxymethyluracil in eukaryote DNA: a natural feature of the Pyrrophyta (dinoflagellates). Science 194: 1062-1064.
95. RAE, P. M. M., AND R. E. STEELE. 1978. Modified bases in the DNAs of unicellular eukaryotes: and examination of distribution and possible roles, with emphasis on hydroxymethyluracil in dinoflagellates. BioSystems 10: 37-53.
96. RAGELIS, E. P. 1984. Ciguatera seafood poisoning: overview. In E. P. Ragelis [ed.], Seafood toxins, 25-36. American Chemical Society Symposium Series no. 262, Washington, D.C., USA.
97. REHKOPF, D. H., D. E. GILLESPIE, M. I. HARRELL, AND J. E. FEAGIN. 2000. Transcriptional mapping and RNA processing of the Plasmodium falciparum mitochondrial mRNAs. Molecular and Biochemical Parasitology 105: 91-103.
98. RIZZO, P. J. 1981. Comparative aspects of basic chromatin proteins in dinoflagellates. BioSystems 14: 433-443.
99. RIZZO, P. J. 1991. The enigma of the dinoflagellate chromosome. Journal of Protozoology 38: 246-252.
100. ROWAN, R., AND D. A. POWERS. 1992. Ribosomal RNA sequences and the diversity of symbiotic dinoflagellates. Proceedings of the National Academy of Sciences, USA 89: 3639-3643.
101. SAKO, Y., T. YOSHIDA, A. UCHIDA, O. ARAKAWA, T. NOGUCHI, AND Y. ISHIDA. 2001. Purification and characterization of a sulfotransferase specific to N-21 of saxitoxin and gonyautoxin 2 + 3 from the toxic dinoflagellate Gymodinium catenatum (Dinophyceae). Journal of Phycology 37: 1044-1051.
102. SALDARRIAGA, J. F., F. J. R. TAYLOR, P. J. KEELING, AND T. CAVALIER-SMITH. 2001. Dinoflagellate nuclear SSU rDNA phylogeny suggests multiple plastid losses and replacements. Journal of Molecular Evolution 53: 204-213.
103. SALDARRIAGA, J. F., M. L. MCEWAN, N. M. FAST, F. J. R. TAYLOR, AND P. J. KEELING. 2003. Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage. International Journal of Systematic and Evolutionary Microbiology 53: 355-365.
104. SAUNDERS, G. W., D. R. A. HILL, J. P. SEXTON, AND R. A. ANDERSEN. 1997. Small subunit ribosomal RNA sequences from selected dinoflagellates: testing classical evolutionary hypotheses with molecular systematic methods. In D. Bhattacharya [ed.], Origins of algae and their plastids, 237-259. Springer-Verlag,Vienna, Austria.
105. SCHNEPF, E. 1993. From prey via endosymbiont to plastid: comparative studies in dinoflagellates. In R. A. Lewin [ed.], Origins of plastids, 53-76. Chapman and Hall, New York, New York, USA.
106. 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.
107. SCHNEPF, E., AND M. ELBRÄCHTER. 1999. Dinophyte chloroplasts and phylogeny - a review. Grana 38: 81-97.
108. SHUMWAY, S. E. 1989. Toxic algae: a serious threat to shellfish aquaculture. World Aquaculture 20: 65-74.
109. SIGEE, D. C. 1984. Structural DNA and genetically active DNA in dinoflagellate chromosomes. Biosystems 16: 203-210.
110. SILVA, E. S. 1978. Endonuclear bacteria in two species of dinoflagellates. Protistologica 14: 113-119.
111. SMAYDA, T. J. 1997. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnology and Oceanography 42: 1137-1153.
112. SOYER, M. O., AND O. K. HAAPALA. 1974. Structural changes of dinoflagellate chromosome by pronase and ribonuclease. Chromosoma 47: 179-192.
113. SOYER-GOBILLARD, M. O., M. L. GERAUD, D. COULAUD, M. BARRAY, B. THEVENY, B. REVET, AND E. DELAIN. 1990. Location of B- and Z-DNA in the chromosomes of a primitive eukaryote dinoflagellate. Journal of Cell Biology 111: 293-308.
114. SPECTOR, D. L. 1984. Dinoflagellate nuclei. In D. L. Spector [ed.], Dinoflagellates, 107-147. Academic Press, Inc., Orlando, Florida, USA.
115. STANLEY, G. D., AND P. K. SWART. 1995. Evolution of the coral-zooxanthella synbiosis during the Triassic: a geochemical approach. Paleobiology 21: 179-199.
116. STEIDINGER, K. A. 1983. A re-evaluation of toxic dinoflagellate biology and ecology. In F. E. Round and V. J. Chapman [eds.], Progress in phycological research, vol. 2, 147-188. Elsevier, New York, New York, USA.
117. SWEENEY, B. M. 1987. Bioluminescence and circadian rhythms. In F. J. R. Taylor [ed.], The biology of dinoflagellates, 269-281. Blackwell, Oxford, UK.
118. 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.
119. TARONCHER-OLDENBURG, G., AND D. M. ANDERSON. 2000. Identification and characterization of three differentially expressed genes, encoding Sadenosylhomocysteine hydrolase, methionine aminopeptidase, and a histone-like protein, in the toxic dinoflagellate Alexandrium fundyense. Applied and Environmental Microbiology 66: 2105-2112.
120. 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 199hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Molecular Biology and Evolution 17: 718-729.
121. TRENCH, R. K. 1987. Dinoflagellates in non-parasitic symbioses. In F. J. R. Taylor [ed.], The biology of dinoflagellates, 530-570. Blackwell, Oxford, UK.
122. TRENCH, R. K. 1993. Microalgal-invertebrate symbioses: a review. Endocytobiosis and Cell Research 9: 135-175.
123. TRENCH, R. K. 1997. Diversity of symbiotic dinoflagellates and the evolution of microalgal-invertebrate symbioses. In H. A. Lessios and I. G. Macintyre [eds.], Proceedings of the Eighth International Coral Reef Symposium, 2: 1275-1286. Smithsonian Tropical Research Institute, Balboa, Panama.
124. TRIPLETT, E. L., R. V. M. JOVINE, N. S. GOVIND, S. J. ROMAN, S. S. CHANG, AND B. B. PREZELIN. 1993. Characterization of two full-length cDNA sequences encoding for apoproteins of peridinin-chlorophyll a-protein (PCP) complexes. Molecular Marine Biology and Biotechnology 2: 246-254.
125. USUP, G., D. M. KULIS, AND D. M. ANDERSON. 1994. Growth and toxin production of the toxic dinoflagellate Pyrodinium bahamense var. compressum in laboratory cultures. Natural Toxins 2: 254-262.
126. VAN DE PEER, Y., AND R. DE WACHTER. 1997. Evolutionary relationships among the eukaryotic crown taxa taking into account site-to-site rate variation in 18S rDNA. Journal of Molecular Evolution 45: 619-630.
127. VAN DOLAH, F. M. 2000. Marine algal toxins: origins, health effects, and their increased occurrence. Environmental Health Perspectives 108(Supplement 1): 133-141.
128. VASQUEZ, M., C. GRUTTNER, S. GALLACHER, AND E. R. B. MOORE. 2001. Detection and characterization of toxigenic bacteria associated with Alexandrium catenella and Aulacomya ater contaminated with PSP. Journal of Shellfish Research 20: 1245-1249.
129. VERNET, G., M. SALA-ROVIRA, M. MAEDER, F. JACQUES, AND M. HERZOG. 1990. Basic nuclear proteins of the histone-less eukaryote Crypthecodinium cohnii (Pyrrophyta): two-dimensional electrophoresis and DNAbinding properties. Biochimica et Biophysica Acta 1048: 281-289.
130. VESK, M., T. P. DIBBAYAWAN, AND P. A. VESK. 1996. Immunogold localization of phycoerythrin in chloroplasts of Dinophysis acuminata and D. fortii (Dinophysiales, Dinophyta). Phycologia 35: 234-238.
131. VOLKMAN, J. K., P. KEARNEY, AND S. W. JEFFREY. 1990. A new source of 4-methyl sterols and 5(H)-stanols in sediments: prymnesiophyte microalgae of the genus Pavlova. Organic Geochemistry 15: 489-497.
132. 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.
133. WATANABE, M. M., Y. TAKEDA, T. SASA, I. INOUYE, 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.
134. WATANABE, M. M., T. SASA, S. SUDA, I. INOUYE, AND S. TAKICHI. 1991. Major carotenoid composition of an endosymbiont is a green dinoflagellate, Lepidodinium viride. Journal of Phycology 27: 75.
135. WHITNEY, S. M., D. C. SHAW, AND D. YELLOWLEES. 1995. Evidence that some dinoflagellates contain a ribulose-1,5-bisphosphate carboxylase/oxygenase related to that of the alpha-proteobacteria. Proceedings of the Royal Society of London, series B 259: 271-275.
136. WITHERS, N. 1987. Dinoflagellate sterols. In F. J. R. Taylor [ed.], The biology of dinoflagellates, 316-359. Blackwell, Oxford, UK.
137. WITHERS, N. W., E. R. COX, R. TOMAS, AND F. T. HAXO. 1977. Pigments of the dinoflagellate Peridinium balticum and its photosynthetic endosymbiont. Journal of Phycology 13: 354-358.
138. YEN, C. S., R. E. STEELE, AND P. M. M. RAE. 1978. Chromatin structure in a dinoflagellate as revealed by electron microscopy of DNA cross-linked in vivo with trimethylpsoralen. Journal of Cell Biology 79: 120a.
139. 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.
140. YOON, H. S., J. HACKETT, C. CINIGLIA, G. PINTO, AND D. BHATTACHARYA. 2004. A molecular timeline for the origin of photosynthetic eukaryotes. Molecular Biology and Evolution 21: 809-818.
141. ZHANG, Z., B. R. GREEN, AND T. CAVALIER-SMITH. 1999. Single gene circles in dinoflagellate chloroplast genomes. Nature 400: 155-159.
142. ZHANG, Z., T. CAVALIER-SMITH, AND B. R. GREEN. 2002. Evolution of dinoflagellate unigenic minicircles and the partially concerted divergence of their putative replicon origins. Molecular Biology and Evolution 19: 489-500.