Plastid Endosymbiosis. Sources and Timing of the Major Events.

Evolution of Primary Producers in the Sea

Volumn , Issue , 2007, Pages 109-132

  Hackett, Jeremiah D ^a   Su Yoon, Hwan ^b   Butterfield, Nicholas J ^c   Sanderson, Michael J ^d   Bhattacharya, Debashish ^b  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84882509169     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-012370518-1/50008-4     Document Type: Chapter

References (121)

1. Adl S.M., Simpson A.G., Farmer M.A. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 2005, 52:399-451. and 25 others.
2. Allen J.F., Puthiyaveetil S., Strom J., Allen C.A. Energy transduction anchors genes in organelles. Bioessays 2005, 27:426-435.
3. Allen J.F., Raven J.A. Free-radical-induced mutation vs redox regulation: costs and benefits of genes in organelles. J. Mol. Evol. 1996, 42:482-492.
4. Arisue N., Hasegawa M., Hashimoto T. Root of the Eukaryota tree as inferred from combined maximum likelihood analyses of multiple molecular sequence data. Mol. Biol. Evol. 2005, 22:409-420.
5. Arisue N., Hashimoto T., Yoshikawa H., Nakamura G., Nakamura F., Yano T.A., Hasegawa M. Phylogenetic position of Blastocystis hominis and of stramenopiles inferred from multiple molecular sequence data. J. Eukaryot. Microbiol. 2002, 49:42-53.
6. Azam F., Fenchel T., Field J.G., Gray J.S., Meyer-Reil L.A., Thingstad F. The ecological role of water column microbes in the sea. Mar. Ecol. Prog. Ser. 1983, 10:257-264.
7. Bachvaroff T.R., Sanchez Puerta M.V., Delwiche C.F. Chlorophyll c containing plastid relationships based on analyses of a multi-gene dataset with all four chromalveolate lineages. Mol. Biol. Evol. 2005, 22:1772-1782.
8. Baldauf S.L., Roger A.J., Wenk-Siefert I., Doolittle W.F. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 2000, 290:972-977.
9. Barbier G., Oesterhelt C., Larson M.D., Halgren R.G., Wilkerson C., Garavito R.M., Benning C., Weber A.P. Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular. Plant Physiol 2005, 137:460-474.
10. Barbrook A.C., Howe C.J. Minicircular plastid DNA in the dinoflagellate Amphidinium operculatum. Mol. Gen. Genet. 2000, 263:152-158.
11. Benton M.J. Fossil Record 2 1993, Chapman and Hall, London.
12. Bhattacharya D., Helmchen T., Melkonian M. Molecular evolutionary analyses of nuclear-encoded small subunit ribosomal RNA identify an independent rhizopod lineage containing the Euglyphina and the Chlo. J. Eukaryot. Microbiol. 1995, 42:65-69.
13. Bhattacharya D., Medlin L.K. The phylogeny of plastids: a review based on comparisons of small-subunit ribosomal RNA coding regions. J. Phycol. 1995, 31:489-498.
14. Bhattacharya D., Yoon H.S., Hackett J.D. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays 2004, 26:50-60.
15. Blair J.E., Shah P., Hedges S.B. Evolutionary sequence analysis of complete eukaryote genomes. BMC Bioinformatics 2005, 6:53.
16. Bowe L.M., Coat G., dePamphilis C.W. Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales' closest relatives are conifers. Proc. Natl. Acad. Sci. U S A 2000, 97:4092-4097.
17. Brasier M.D., Lindsay J.F. A billion years of environmental stability and the emergence of eukaryotes: new data from northern Australia. Geology 1998, 26:555-558.
18. Brocks J.J., Logan G.A., Buick R., Summons R.E. Archean molecular fossils and the early rise of eukaryotes. Science 1999, 285:1033-1036.
19. Brocks J.J., Love G.D., Summons R.E., Knoll A.H., Logan G.A., Bowden S.A. Biomarker evidence for green and purple sulphur bacteria in a stratified Palaeoproterozoic sea. Nature 2005, 437:866-870.
20. Buick R., Thornett J.R., McNaughton N.J., Smith J.B., Barley M.E., Savage M. Record of emergent continental crust similar to 3.5 billion years ago in the Pilbara craton in Australia. Nature 1995, 375:574-577.
21. Butterfield N.J. Paleobiology of the late Mesoproterozoic (ca. 1200 Ma) Hunting Formation, Somerset Island, arctic Canada. Precambrian Res. 2001, 111:235-256.
22. Butterfield N.J. A vaucheriacean alga from the middle Neoproterozoic of Spitsbergen: implications for the evolution of Proterozoic eukaryotes and the Cambrian explosion. Paleobiology 2004, 30:231-252.
23. Butterfield N.J. Probable Proterozoic fungi. Paleobiology 2005, 31:165-182.
24. Cavalier-Smith T. The kingdom Chromista: origin and systematics. Progress in Phycological Research 1986, 309-347. Biopress, Bristol. F. E. Round, D. J. Chapman (Eds.).
25. Cavalier-Smith T. Kingdom Protozoa and its 18 phyla. Microbiol. Rev. 1993, 57:953-994.
26. Cavalier-Smith T. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J. Euk. Microbiol 1999, 46:347-366.
27. Cavalier-Smith T. Membrane heredity and early chloroplast evolution. Trends Plant Sci. 2000, 5:174-182.
28. Cavalier-Smith T. The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int. J. Syst. Evol. Microbiol 2002, 52:7-76.
29. Delwiche C.F. Tracing the thread of plastid diversity through the tapestry of life. Am. Nat. 1999, 154:S164-S177.
30. Delwiche C.F. The origin and evolution of dinoflagellates. Evolution of Primary Producers in the Sea 2007, 191-205. Elsevier, Boston. P.G. Falkowski, A.H. Knoll (Eds.).
31. Douglas S., Zauner S., Fraunholz M., Beaton M., Penny S., Deng L.T., Wu X., Reith M., Cavalier-Smith T, Maier U.G. The highly reduced genome of an enslaved algal nucleus. Nature 2001, 410:1091-1096.
32. Douzery E.J., Snell E.A., Bapteste E., Delsuc E, Philippe H. The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils?. Proc. Natl. Acad. Sci. U S A 2004, 101:15386-15391.
33. Durnford D.G., Deane J.A., Tan S., McFadden G.I., Gantt E., Green B.R. A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J. Mol. Evol. 1999, 48:59-68.
34. Fast N.M., Kissinger J.C., Roos D.S., Keeling P.J. Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol. Biol. Evol. 2001, 18:418-426.
35. Flügge U.I. Metabolite transporters in plastids. Curr. Opin. Plant Biol. 1998, 1:201-206.
36. Funes S., Davidson E., Reyes-Prieto A., Magallon S., Herion P., King M.P., Gonzalez-Halphen D. A green algal apicoplast ancestor. Science 2002, 298:2155.
37. Gibbs S.P The chloroplast of Euglena may have evolved from symbiotic green algae. Can. J. Bot. 1978, 56:2883-2889.
38. Gilson P.R., McFadden G.I. The miniaturized nuclear genome of eukaryotic endosymbiont contains genes that overlap, genes that are cotranscribed, and the smallest known spliceosomal intr. Proc. Natl. Acad. Sci. U S A 1996, 93:7737-7742.
39. Goldman N., Anderson J.P., Rodrigo A.G. Likelihood-based tests of topologies in phylogenetics. Syst. Biol. 2000, 49:652-670.
40. Gray M.W. The endosymbiont hypothesis revisited. Int. Rev. Cyt. 1992, 141:233-357.
41. Greenwood A.D. The Cryptophyta in relation to phylogeny and photosynthesis. Electron Microscopy 1974 1974, 566-567. Australian Academy of Sciences, Canberra. D.J. Goodchild (Ed.).
42. Guindon S., Gascuel O. PHYML-A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
43. Hackett J.D., Anderson D.M., Erdner D.L., Bhattacharya D. Dinoflagellates: a remarkable evolutionary experiment. Am. J. Bot. 2004, 91:1523-1534.
44. Hackett J.D., Yoon H.S., Soares M.B., Bonaldo M.F., Casavant T.L., Scheetz T.E., Nosenko T., Bhattacharya D. Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Curr. Biol. 2004, 14:213-218.
45. Hagopian J.C., Reis M., Kitajima J.P., Bhattacharya D., de Oliveira M.C. Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui provides insights into the evolution of rhodo. J. Mol. Evol. 2004, 59:464-477.
46. Han T.M., Runnegar B. Megascopic eukaryotic algae from the 2.1-billion-year-old negaunee iron-formation, Michigan. Science 1992, 257:232-235.
47. Harper J.T., Keeling P.J. Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol. Biol. Evol. 2003, 20:1730-1735.
48. Hedges S.B., Blair J.E., Venturi M.L., Shoe J.L. A molecular timescale of eukaryotic evolution and the rise of complex multicellular life. BMC Evol. Biol. 2004, 4:2.
49. Hermann T.N. Organic World Billion Year Ago 1990, 1-49. Nauka, Leningrad.
50. Hiller R.G. "Empty" minicircles and petB/atpA and psbD/psbE (cytb559 alpha) genes in tandem in Amphidinium carterae plastid DNA. FEBS Lett. 2001, 505:449-452.
51. Holder M.E., Roger A.J. PUZZLEBOOT 1999, Available online at. http://www.hades.biochem.dal.ca/Rogerlab/Software/software.html#puzzlebo ot.
52. Huelsenbeck J.P., Ronquist F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
53. Huntley J.W., Xiao S., Kowalewski M. 1.3 Billion years of acritarch history: An empirical morphospace approach. Precambrian Res. 2006, 144:52-68.
54. Javaux E.J., Knoll A.H., Walter M.R. Morphological and ecological complexity in early eukaryotic ecosystems. Nature 2001, 412:66-69.
55. Johnson P.W., Hargraves P.E., Sieburth J.M. Ultrastructure and ecology of Calycomonas ovalis Wulff, 1919, (Chrysophyceae) and its redescription as a testate rhizopod, Paulinella ovalis n. comb. (Filosea. J. Protozool. 1988, 35:618-626.
56. Jones D.T., Taylor W.R., Thornton J.M. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 1992, 8:275-282.
57. Kenrick P., Crane PR. The origin and early evolution of plants on land. Nature 1997, 389:33-39.
58. Kies L. Elektronenmikroskopische Untersuchungen an Paulinella chromatophora Lauterborn, einer Thekamöbe mit blaugrünen Endosymbionten (Cyanellen). Protoplasma 1974, 80:69-89.
59. Kies L., Kremer B.P. Phylum Glaucocsytophyta. Handbook of Protoctista 1990, 152-166. Jones and Bartlett, Boston. L. Margulis, J.O. Corliss, M. Melkonian, D.J. Chapman (Eds.).
60. Kishino H., Hasegawa M. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J. Mol. Evol. 1989, 29:170-179.
61. Kishino H., Thorne J.L., Bruno W.J. Performance of a divergence time estimation method under a probabilistic model of rate evolution. Mol. Biol. Evol. 2001, 18:352-361.
62. Knoll A.H. Proterozoic and early Cambrian protists: evidence for accelerating evolutionary tempo. Proc. Natl. Acad. Sci. U S A 1994, 91:6743-6750.
63. Knoll A.H., Summon F.E., Waldbauer J.R., Zumberge J.E. The geological succession of primary producers in the sea. Evolution of Primary Producers in the Sea 2007, 133-163. Elsevier, Boston. P.G. Falkowski, A.H. Knoll (Eds.).
64. Köhler S., Delwiche C.F., Denny P.W., Tilney L.G., Webster P., Wilson R.J., Palmer J.D., Roos D.S. A plastid of probable green algal origin in Apicomplexan parasites. Science 1997, 275:1485-1489.
65. Koike K., Sekiguchi H., Kobiyama A., Takishita K., Kawachi M., Koike K., Ogata T. A novel type of kleptoplastidy in Dinophysis (Dinophyceae): Presence of haptophyte-type plastid in Dinophysis mitra. Protist 2005, 156:225-237.
66. Laatsch T., Zauner S., Stoebe-Maier B., Kowallik K.V., Maier U.G. Plastid-derived single gene minicircles of the dinoflagellate Ceratium horridum are localized in the nucleus. Mol. Biol. Evol. 2004, 21:1318-1322.
67. Li S., Nosenko T., Hackett J.D., Bhattacharya D. Phylogenomic analysis identifies red algal genes of enosymbiotic origin in the chromalveolates. Mol. Biol. Evol. 2005, 23:663-674.
68. Marin B., Nowack E.C.M., Melkonian M. A plastid in the making: evidence for a second primary endosymbiosis. Protist 2005, 156:425-432.
69. Martin W. Eukaryote and mitochondrial origins: Two sides of the same coin and too much ado about oxygen. Evolution of Primary Producers in the Sea 2007, 55-73. Elsevier, Boston. P.G. Falkowski, A.H. Knoll (Eds.).
70. Martin W., Herrmann R.G. Gene transfer from organelles to the nucleus: how much, what happens, and why?. Plant Physiol 1998, 118:9-17.
71. Martin W., Rotte C., Hoffmeister M., Thiessen U., Gelius-Dietrich G., Ahr S., Henze K. Early cell evolution, eukaryotes, anoxia, sulfide, oxygen, fungi first (?), and a tree of genomes revisited. IUBMB Life 2003, 55:193-204.
72. Martin W., Rujan T., Richly E., Hansen A., Cornelsen S., Lins T., Lesister D., Stoebe B., Hasegawa M., Penny D. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl. Acad. Sci. U S A 2002, 99:12246-12251.
73. Martin W., Stoebe B., Goremykin V., Hansmann S., Hasegawa M., Kowallik K. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 1998, 393:162-165.
74. Matsuzaki M., Misumi O., Shin I.T. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 2004, 428:653-657. and 39 others.
75. McFadden G.I. Primary and secondary endosymbiosis and the origin of plastids. J. Phycol 2001, 37:951-959.
76. McFadden G.I., Gilson PR., Hofmann C.J.B., Adcock G.J., Maier U.G. Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga. Proc. Natl. Acad. Sci. U S A 1994, 91:3690-3694.
77. McFadden G.I., van Dooren G.G. Evolution: Red algal genome affirms a common origin of all plastids. Curr. Biol. 2004, 14:R514-R516.
78. McFadden G.I., Waller R.F., Reith M.E., Lang-Unnasch N. Plastids in apicomplexan parasites. Origin of Algae and Their Plastids 1997, 261-287. Springer-Wein, New York. D. Bhattacharya (Ed.).
79. Miyagishima S.Y., Nozaki H., Nishida K., Matsuzaki M., Kuroiwa T. Two types of FtsZ proteins in mitochondria and red-lineage chloroplasts: the duplication of FtsZ is implicated in endosymbiosis. J. Mol. Evol. 2004, 58:291-303.
80. Moreira D., Le Guyader H., Phillippe H. The origin of red algae and the evolution of chloroplasts. Nature 2000, 405:69-72.
81. Muller H.J. Some genetic aspects of sex. Am. Nat. 1932, 66:118-138.
82. Nassoury N., Cappadocia M., Morse D. Plastid ultrastructure defines the protein import pathway in dinoflagellates. J. Cell Sci. 2003, 116:2867-2874.
83. Nelson N., Ben-Shem A. The complex architecture of oxygenic photosynthesis. Nat. Rev. Mol. Cell Biol. 2004, 5:971-982.
84. Nisbet R.E., Koumandou L.V., Barbrook A.C., Howe C.J. Novel plastid gene minicircles in the dinoflagellate Amphidinium operculatutn. Gene 2004, 331:141-147.
85. Nosenko, T., Lidie, K.L., Van Dolah, RM., Lindquist, E., Cheng, J.-F., U.S. Department of Energy-Joint Genome Institute, and Bhattacharya, D. (In press). Chim.
86. Ohta N., Matsuzaki M., Misumi O., Miyagishima S.Y., Nozaki H., Tanaka K., Shin I.T., Kohara Y., Kuroiwa T. Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res. 2003, 10:67-77.
87. Okamoto N., Inouye I. A secondary symbiosis in progress?. Science 2005, 310:287.
88. Palmer J.D. The symbiotic birth of plastids: How many times and whodunit?. J. Phycol. 2003, 39:4-11.
89. Peterson K.J., Butterfield N.J. Origin of the Eumetazoa: testing ecological predictions of molecular clocks against the Proterozoic fossil record. Proc. Natl. Acad. Sci. U S A 2005, 102:9547-9552.
90. Pfanzagl B., Zenker A., Pittenauer E., Allmaier G., Martinez-Torrecuadrada J., Schmidt E.R., Depedro J.A., Löffelhardt W. Primary structure of cyanelle peptidoglycan of Cyanophora paradoxa: a prokaryotic cell wall as part of an organelle envelope. J. Bacteriol. 1996, 178:332-339.
91. Reumann S., Inoue K., Keegstra K. Evolution of the general protein import pathway of plastids. Mol. Membr. Biol. 2005, 22:73-86.
92. Reyes-Prieto, A., and Bhattacharya, D. Phylogeny of nuclear encoded plastid targeted proteins demonstrates an early divergence of glaucophytes within plantae.
93. Rodriguez-Ezpeleta N., Brinkmann H., Burey S.C., Roure B., Burger G., Löffelhardt W., Bohnert HJ., Philippe H., Lang B.F. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr. Biol. 2005, 15:1325-1330.
94. Samuelsson J., Butterfield N.J. Neoproterozoic fossils from the Franklin Mountains, northwestern Canada: stratigraphic and palaeobiological implications. Precambrian Res. 2001, 107:235.
95. Sanchez Puerta M.V., Bachvaroff T.R., Delwiche C.F. The complete mitochondrial genome sequence of the haptophyte Emiliania huxleyi and its relation to heterokonts. DNA Res. 2004, 11:1-10.
96. Sanderson M.J. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 2003, 19:301-302.
97. Sanderson M.J., Doyle J.A. Sources of error and confidence intervals in estimating the age of angiosperms from rbcL and 18S rDNA data. Am. J. Bot. 2001, 88:1499-1516.
98. Schneider D.A., Bickford M.E., Cannon W.R, Schulz K.J., Hamilton M.A. Age of volcanic rocks and syndepositional iron formations, Marquette Range Supergroup: implications for the tectonic setting of Paleoproterozoic iron formatio. Can. J. Earth Sci. 2002, 39:999-1012.
99. Schnepf E., Elbrachter M. Dinophyte chloroplasts and phylogeny-a review. Grana 1999, 38:81-97.
100. Stechmann A., Cavalier-Smith T. Rooting the eukaryote tree by using a derived gene fusion. Science 2002, 297:89-91.
101. Stibitz T.B., Keeling P.J., Bhattacharya D. Symbiotic origin of a novel actin gene in the cryptophyte Pyrenomonas helgolandii. Mol. Biol. Evol. 2000, 17:1731-1738.
102. Summons R.E., Jahnke L.L., Hope J.M., Logan G.A. 2-Methylhopanoids as biomarkers for cyanobacterial oxygenie photosynthesis. Nature 1999, 400:554-557.
103. Swofford D.L. PAUP: Phylogenetic Analysis Using Parsimony ( and Other Methods) 2003, Sunderland, MA, Sinauer.
104. Taylor T.N., Hass H., Kerp H. The oldest fossil ascomycetes. Nature 1999, 399:648.
105. Tengs T., Dahlberg O.J., Shalchian-Tabrizi K., Klaveness D., Rudi K., Delwiche C.F., Jakobsen K.S. Phylogenetic analyses indicate that the 19'Hexanoyloxy-fucoxanthincontaining dinoflagellates have tertiary plastids of haptophyte origin. Mol. Biol. Evol. 2000, 17:718-729.
106. Thorne J.L., Kishino H., Painter I.S. Estimating the rate of evolution of the rate of molecular evolution. Mol. Biol. Evol. 1998, 15:1647-1657.
107. Van De Peer Y., De Wachter R. Evolutionary relationships among the eukaryotic crown taxa taking into account site-to-site rate variation in 18S rRNA. J. Mol. Evol. 1997, 45:619-630.
108. Van De Peer Y., Rensing S.A., Maier U.G., De Wachter R. Substitution rate calibration of small subunit ribosomal RNA identifies chlorarachniophyte endosymbionts as remnants of green algae. Proc. Natl. Acad. Sci. U S A 1996, 93:7732-7736.
109. Watanabe M.M., Sasa T., Suda S., Inouye I., Takichi S. Major carotenoid composition of an endosymbiont is a green dinoflagellate, Lepidodinium viride. J. Phycol 1991, 27:75.
110. Watanabe M.M., Suda S., Inouye I., Sawaguchi T., Chihara M. Lepidodinium viride new genus new species Gymnodiniales Dinophyta a green dinoflagellate with a chlorophyll a-containing and chlorophyll b-containing endosymb. J. Phycol 1990, 26:741-751.
111. Weber A.P.M., Linka M., Bhattacharya D. Single, ancient origin of a plastid metabolite translocator family in Plantae from an endomembrane- derived ancestor. Eukaryot. Cell 2006, 5:609-612.
112. Whelan S., Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 2001, 18:691-699.
113. Yoon H.S., Hackett J.D., Ciniglia C., Pinto G., Bhattacharya D. A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 2004, 21:809-818.
114. Yoon H.S., Hackett J.D., Pinto G., Bhattacharya D. The single, ancient origin of chromist plastids. Proc. Natl. Acad. Sci. U S A 2002, 99:15507-15512.
115. Yoon H.S., Hackett J.D., Van Dolah F.M., Nosenko T., Lidie K.L., Bhattacharya D. Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol. Biol. Evol. 2005, 22:1299-1308.
116. Yoon H.S., Reyes-Prieto A., Melkonian M., Bhattacharya D. Minimal plastid genome evolution in the Paulinella endosymbiont. Curr. Biol. 2006, 16:R670-R672.
117. Zhang Z., Cavalier-Smith T., Green B.R. A family of selfish minicircular chromosomes with jumbled chloroplast gene fragments from a dinoflagellate. Mol. Biol. Evol. 2001, 18:1558-1565.
118. Zhang Z., Cavalier-Smith T., Green B.R. Evolution of dinoflagellate unigenic minicircles and the partially concerted divergence of their putative replicon origins. Mol. Biol. Evol. 2002, 19:489-500.
119. Zhang Z., Green B.R., Cavalier-Smith T. Single gene circles in dinoflagellate chloroplast genomes. Nature 1999, 400:155-159.
120. Nosenko, T., Lidie, K.L., Van Dolah, RM., Lindquist, E., Cheng, J.-F., U.S. Department of Energy-Joint Genome Institute, and Bhattacharya, D. (In press). Chim.
121. Reyes-Prieto, A., and Bhattacharya, D. Phylogeny of nuclear encoded plastid targeted proteins demonstrates an early divergence of glaucophytes within plantae.