The endosymbiotic origin, diversification and fate of plastids

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1541, 2010, Pages 729-748

  Keeling, Patrick J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Algae; Endosymbiosis; Evolution; Phylogeny; Plastids; Protist

Indexed keywords

ANCESTRY; DINOFLAGELLATE; ENDOSYMBIONT; EVOLUTIONARY THEORY; GENE TRANSFER; GREEN ALGA; PHOTOSYNTHESIS; PHYLOGENY; PLASTID;

ALGAE; CHLORARACHNIOPHYCEAE; CHLOROPHYTA; CHROMALVEOLATA; DINOPHYCEAE; EUGLENIDA; EUKARYOTA; GLAUCOCYSTOPHYCEAE; PAULINELLA; PROTISTA; RHIZARIA; RHODOPHYTA;

EID: 77349112000     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0103     Document Type: Review

References (213)

1. Abrahamsen, M. S. et al. 2004 Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304, 441-445. (doi:10.1126/science.1094786)
2. Adl, S. M. et al. 2005 The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52, 399-451. (doi:10.1111/j.1550-7408.2005.00053.x)
3. Archibald, J. M. 2005 Jumping genes and shrinking genomes - probing the evolution of eukaryotic photosynthesis with genomics. IUBMB Life 57, 539-547. (doi:10.1080/15216540500167732)
4. Archibald, J. M. 2007 Nucleomorph genomes: structure, function, origin and evolution. Bioessays 29, 392-402. (doi:10.1002/bies.20551)
5. Archibald, J. M. & Keeling, P. J. 2002 Recycled plastids: a green movement in eukaryotic evolution. Trends Genet. 18, 577-584. (doi:10.1016/S0168-9525(02)02777-4)
6. Archibald, J. M., Longet, D., Pawlowski, J. & Keeling, P. J. 2002 A novel polyubiquitin structure in Cercozoa and Foraminifera: evidence for a new eukaryotic supergroup. Mol. Biol. Evol. 20, 62-66. (doi:10.1093/molbev/msg006)
7. Archibald, J. M., Rogers, M. B., Toop, M., Ishida, K. & Keeling, P. J. 2003 Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc. Natl Acad. Sci. USA 100, 7678-7683. (doi:10.1073/pnas.1230951100)
8. Armbrust, E. V. et al. 2004 The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306, 79-86. (doi:10.1126/science.1101156)
9. Aury, J. M. et al. 2006 Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444, 171-178. (doi:10.1038/nature05230)
10. Bachvaroff, T. R., Concepcion, G. T., Rogers, C. R., Herman, E. M. & Delwiche, C. F. 2004 Dinoflagellate expressed sequence tags data indicate massive trasfer of chloroplast genes to the nuclear genome. Protist 155, 65-78. (doi:10.1078/1434461000165)
11. Barrett, C. F. & Freudenstein, J. V. 2008 Molecular evolution of rbcL in the mycoheterotrophic coralroot orchids (Corallorhiza Gagnebin, Orchidaceae). Mol. Phylogenet. Evol. 47, 665-679. (doi:10.1016/j.ympev.2008.02.014)
12. Bergthorsson, U., Adams, K. L., Thomason, B. & Palmer, J. D. 2003 Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424, 197-201. (doi:10.1038/nature01743)
13. Bergthorsson, U., Richardson, A. O., Young, G. J., Goertzen, L. R. & Palmer, J. D. 2004 Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proc. Natl Acad. Sci. USA 101, 17 747-17 752. (doi:10.1073/pnas.0408336102)
14. Besendahl, A., Qiu, Y. L., Lee, J., Palmer, J. D. & Bhattacharya, D. 2000 The cyanobacterial origin and vertical transmission of the plastid tRNA(Leu) group-I intron. Curr. Genet. 37, 12-23. (doi:10.1007/s002940050002)
15. Bhattacharya, D. & Schmidt, H. A. 1997 Division Glaucocystophyta. In Origin of algae and their plastids (ed. D. Bhattacharya), pp. 139-148. Wien, New York: Springer-Verlag.
16. Bhattacharya, D. & Weber, K. 1997 The actin gene of the glaucocystophyte Cyanophora paradoxa: analysis of the coding region and introns, and an actin phylogeny of eukaryotes. Curr. Genet. 31, 439-446. (doi:10.1007/s002940050227)
17. Bhattacharya, D., Helmchen, T. & Melkonian, M. 1995 Molecular evolutionary analyses of nuclear-encoded small subunit ribosomal RNA identify an independent rhizopod lineage containing the Euglyphidae and the Chlorarachniophyta. J. Eukaryot. Microbiol. 42, 64-68. (doi:10.1111/j.1550-7408.1995.tb01541.x)
18. Bhattacharya, D., Archibald, J. M., Weber, A. P. & Reyes-Prieto, A. 2007 How do endosymbionts become organelles? Understanding early events in plastid evolution. Bioessays 29, 1239-1246. (doi:10.1002/bies. 20671)
19. Bodyl, A., Mackiewicz, P. & Stiller, J. W. 2007 The intracellular cyanobacteria of Paulinella chromatophora: endosymbionts or organelles? Trends Microbiol. 15, 295-296. (doi:10.1016/j.tim.2007.05.002)
20. Bolte,K., Bullmann, L.,Hempel, F., Bozarth, A., Zauner, S.& Maier,U.G. 2009 Protein targeting into secondary plastids. J. Eukaryot. Microbiol. 56, 9-15. (doi:10.1111/j.1550-7408.2008.00370.x)
21. Borza, T., Popescu, C. E. & Lee, R. W. 2005 Multiple metabolic roles for the nonphotosynthetic plastid of the green alga Prototheca wickerhamii. Eukaryot. Cell 4, 253-261. (doi:10.1128/EC.4.2.253-261.2005)
22. Brugerolle, G. & Taylor, F. J. R. 1977 Taxonomy, cytology and evolution of the Mastigophora. In Proc. Fifth Int. Congress of Protozoology (ed. S. H. Hutner), pp. 14-28. New York, NY: Pace University.
23. Burki, F., Shalchian-Tabrizi, K., Minge, M., Skjaeveland, A., Nikolaev, S. I., Jakobsen, K. S. & Pawlowski, J. 2007 Phylogenomics reshuffles the eukaryotic supergroups. PLoS ONE 2, e790. (doi:10.1371/journal. pone.0000790)
24. Burki, F., Shalchian-Tabrizi, K. & Pawlowski, J. 2008 Phylogenomics reveals a new 'megagroup' including most photosynthetic eukaryotes. Biol. Lett. 4, 366-369. (doi:10.1098/rsbl.2008.0224)
25. Burki, F. et al. 2009 Massive sequencing and phylogenomics of two enigmatic protist lineages reveal Telonemia and Centrohelizoa are related to photosynthetic chromalveolates. Genom. Biol. Evol. 1, 231-238.
26. Cavalier-Smith, T. 1982 The origins of plastids. Biol. J. Linn. Soc. 17, 289-306. (doi:10.1111/j.1095-8312.1982.tb02023.x)
27. Cavalier-Smith, T. 1999 Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J. Eukaryot. Microbiol. 46, 347-366. (doi:10.1111/j.1550-7408.1999.tb04614.x)
28. Cavalier-Smith, T. 2004 Chromalveolate diversity and cell megaevolution: interplay of membranes, genomes and cytoskeleton. In Organelles, genomes and eukaryotic evolution (eds R. P. Hirt & D. Horner), pp. 71-103. London, UK: Taylor and Francis.
29. Cavalier-Smith, T. & Chao, E. E. 1997 Sarcomonad ribosomal RNA sequences, Rhizopod phylogeny, and the origin of Euglyphid Amoebae. Arch. Protistenkd. 147, 227-236.
30. Chesnick, J. M., Hooistra, W. H., Wellbrock, U. & Medlin, L. K. 1997 Ribosomal RNA analysis indicates a benthic pennate diatom ancestry for the endosymbionts of the dinoflagellates Peridinium foliaceum and Peridinium balticum (Pyrrhophyta). J. Eukaryot. Microbiol. 44, 314-320. (doi:10.1111/j.1550-7408.1997.tb05672.x)
31. Cho, Y., Qiu, Y. L., Kuhlman, P. & Palmer, J. D. 1998 Explosive invasion of plant mitochondria by a group I intron. Proc. Natl Acad. Sci. USA 95, 14 244-14 249. (doi:10.1073/pnas.95.24.14244)
32. Cuvelier, M. L., Ortiz, A., Kim, E., Moehlig, H., Richardson, D. E., Heidelberg, J. F., Archibald, J. M. & Worden, A. Z. 2008 Widespread distribution of a unique marine protistan lineage. Environ. Microbiol. 10, 1621-1634. (doi:10.1111/j.1462-2920.2008.01580.x)
33. de Koning, A. P. & Keeling, P. J. 2004 Nucleus-encoded genes for plastid-targeted proteins in Helicosporidium: functional diversity of a cryptic plastid in a parasitic alga. Eukaryot. Cell 3, 1198-1205. (doi:10.1128/EC.3.5.1198-1205.2004)
34. de Koning, A. P. & Keeling, P. J. 2006 The complete plastid genome sequence of the parasitic green alga, Helicosporidium sp. is highly reduced and structured. BMC Biol. 4, 12. (doi:10.1186/1741-7007-4- 12)
35. Delwiche, C. F. 1999 Tracing the thread of plastid diversity through the tapestry of life. Am. Nat. 154(Suppl.), S164-S177. (doi:10.1086/303291)
36. Delwiche, C. F. & Palmer, J. D. 1996 Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol. Biol. Evol. 13, 873-882.
37. Delwiche, C. F., Kuhsel, M. & Palmer, J. D. 1995 Phylogenetic analysis of tufA sequences indicates a cyanobacterial origin of all plastids. Mol. Phylogenet. Evol. 4, 110-128. (doi:10.1006/mpev. 1995.1012)
38. Dodge, J. D. 1969 Observatons on the fine structure of the eyespot and associated organelles in the dinoflagellate Glenodinium foliaceum. J. Cell Sci. 5, 479-493.
39. Dougherty, E. C. & Allen, M. B. 1960 Is pigmentation a clue to protistan phylogeny? In Comparative biochemistry of photoreactive systems (ed. M. B. Allen). New York, NY: Academic Press.
40. Douglas, S. E. 1998 Plastid evolution: origins, diversity, trends. Curr. Opin. Genet. Dev. 8, 655-661. (doi:10.1016/S0959-437X(98) 80033-6)
41. Douglas, A. E. & Raven, J. A. 2003 Genomes at the interface between bacteria and organelles. Phil. Trans. R. Soc. Lond. B 358, 5-18. (doi:10.1098/rstb.2002.1188)
42. Douglas, S. E., Murphy, C. A., Spencer, D. F. & Gray, M.W. 1991Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350, 148-151. (doi:10.1038/350148a0)
43. Douglas, S. et al. 2001 The highly reduced genome of an enslaved algal nucleus. Nature 410, 1091-1016. (doi:10.1038/35074092)
44. Durnford, D. G. & Gray, M. W. 2006 Analysis of Euglena gracilis plastid-targeted proteins reveals different classes of transit sequences. Eukaryot. Cell 5, 2079-2091. (doi:10.1128/EC.00222-06)
45. Durnford, D. G., Deane, J. A., Tan, S., McFadden, G. I., Gantt, E. & Green, B. R. 1999 A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J. Mol. Evol. 48, 59-68. (doi:10.1007/PL00006445)
46. Eisen, J. A. et al. 2006 Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol. 4, e286. (doi:10.1371/journal.pbio.0040286)
47. Elias, M., Patron, N. J. & Keeling, P. J. 2009 The RAB family GTPase Rab1A from Plasmodium falciparum defines a unique paralog shared by chromalveolates and rhizaria. J. Eukaryot. Microbiol. 56, 348-356. (doi:10.1111/j.1550-7408.2009.00408.x)
48. Falkowski, P. G., Katz, M. E., Knoll, A. H., Quigg, A., Raven, J. A., Schofield, O. & Taylor, F. J. 2004 The evolution of modern eukaryotic phytoplankton. Science 305, 354-360. (doi:10.1126/science.1095964)
49. Fast, N. M., Kissinger, J. C., Roos, D. S. & Keeling, P. J. 2001 Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol. Biol. Evol. 18, 418-426.
50. Foth, B. J. & McFadden, G. I. 2003 The apicoplast: a plastid in Plasmodium falciparum and other apicomplexan parasites. Int. Rev. Cytol. 224, 57-110. (doi:10.1016/S0074-7696(05)24003-2)
51. Foth, B. J., Ralph, S. A., Tonkin, C. J., Struck, N. S., Fraunholz, M., Roos, D. S., Cowman, A. F. & McFadden, G. I. 2003 Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299, 705-708. (doi:10.1126/science.1078599)
52. Funes, S., Davidson, E., Reyes-Prieto, A., Magallón, S., Herion, P., King, M. P. & Gonzalez-Halphen, D. 2002 A green algal apicoplast ancestor. Science 298, 2155. (doi:10.1126/science.1076003)
53. Gast, R. J., Moran, D. M., Dennett, M. R. & Caron, D. A. 2007 Kleptoplasty in an Antarctic dinoflagellate: caught in evolutionary transition? Environ. Microbiol. 9, 39-45. (doi:10.1111/j.1462-2920.2006.01109. x)
54. Gibbs, S. P. 1978 The chloroplasts of Euglena may have evolved from symbiotic green algae. Can. J. Bot. 56, 2883-2889. (doi:10.1139/b78-345)
55. Gibbs, S. P. 1981 The chloroplast endoplasmic reticulum: structure, function, and evolutionary significance. Int. Rev. Cytol. 72, 49-99. (doi:10.1016/S0074-7696(08)61194-8)
56. Gile, G. H. & Keeling, P. J. 2008 Nucleus-encoded periplastid-targeted EFL in chlorarachniophytes. Mol. Biol. Evol. 25, 1967-1977. (doi:10.1093/molbev/msn147)
57. Gilson, P. R. & McFadden, G. I. 1996 The miniaturized nuclear genome of a eukaryotic endosymbiont contains genes that overlap, genes that are cotranscribed, and the smallest known spliceosomal introns. Proc. Natl Acad. Sci. USA 93, 7737-7742. (doi:10.1073/pnas.93.15.7737)
58. Gilson, P. R. & McFadden, G. I. 1999 Molecular, morphological and phylogenetic characterization of six chlorarachniophyte strains. Phycol. Res. 47, 7-19. (doi:10.1111/j.1440-1835.1999.tb00278.x)
59. Gilson, P. R. & McFadden, G. I. 2002 Jam packed genomes - a preliminary, comparative analysis of nucleomorphs. Genetica 115, 13-28. (doi:10.1023/A:1016011812442)
60. Gilson, P. R., Su, V., Slamovits, C. H., Reith, M. E., Keeling, P. J. & McFadden, G. I. 2006 Complete nucleotide sequence of the chlorarachniophyte nucleomorph: nature's smallest nucleus. Proc. Natl Acad. Sci. USA 103, 9566-9571. (doi:10.1073/pnas.0600707103)
61. Gogarten, M. B., Gogarten, J. P. & Olendzenski, L. (eds) 2009 Horizontal gene transfer: genomes in flux. New York, NY: Humana Press.
62. Goodman, C. D. & McFadden, G. I. 2008 Fatty acid synthesis in protozoan parasites: unusual pathways and novel drug targets. Curr. Pharm. Des. 14, 901-916. (doi:10.2174/138161208784041088)
63. Gould, S. B., Sommer, M. S., Hadfi, K., Zauner, S., Kroth, P. G. & Maier, U. G. 2006a Protein targeting into the complex plastid of cryptophytes. J. Mol. Evol. 62, 674-681. (doi:10.1007/s00239-005- 0099-y)
64. Gould, S. B., Sommer, M. S., Kroth, P. G., Gile, G. H., Keeling, P. J. & Maier, U. G. 2006b Nucleus-to-nucleus gene transfer and protein retargeting into a remnant cytoplasm of cryptophytes and diatoms. Mol. Biol. Evol. 23, 2413-2422. (doi:10.1093/molbev/msl113)
65. Gould, S. B., Waller, R. F. & McFadden, G. I. 2008 Plastid evolution. Annu. Rev. Plant Biol. 59, 491-517. (doi:10.1146/annurev.arplant. 59.032607.092915)
66. Graham, L. E. & Wilcox, L. W. 2000 Algae. Upper Saddle River, NJ: Prentice-Hall.
67. Grauvogel, C., Reece, K. S., Brinkmann, H. & Petersen, J. 2007 Plastid isoprenoid metabolism in the oyster parasite Perkinsus marinus connects dinoflagellates and malaria pathogens - new impetus for studying alveolates. J. Mol. Evol. 65, 725-729. (doi:10.1007/s00239-007- 9053-5)
68. Gray, M. W. 1999 Evolution of organellar genomes. Curr. Opin. Genet. Dev. 9, 678-687. (doi:10.1016/S0959-437X(99)00030-1)
69. Gray, M. W., Burger, G. & Lang, B. F. 1999 Mitochondrial evolution. Science 283, 1476-1481. (doi:10.1126/science.283.5407.1476)
70. Greenwood, A. D., Griffiths, H. B. & Santore, U. J. 1977 Chloroplasts and cell compartments in Cryptophyceae. Br. Phycol. J. 12, 119.
71. Gross, W., Lenze, D., Nowitzki, U., Weiske, J. & Schnarrenberger, C. 1999 Characterization, cloning, and evolutionary history of the chloroplast and cytosolic class I aldolases of the red alga Galdieria sulphuraria. Gene 230, 7-14. (doi:10.1016/S0378-1119(99)00059-1)
72. Hackett, J. D., Anderson, D. M., Erdner, D. L. & Bhattacharya, D. 2004a Dinoflagellates: a remarkable evolutionary experiment. Am. J. Bot. 91, 1523-1534. (doi:10.3732/ajb.91.10.1523)
73. Hackett, J. D., Yoon, H. S., Soares, M. B., Bonaldo, M. F., Casavant, T. L., Scheetz, T. E., Nosenko, T. & Bhattacharya, D. 2004b Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Curr. Biol. 14, 213-218.
74. Hackett, J. D., Yoon, H. S., Li, S., Reyes-Prieto, A., Rummele, S. E. & Bhattacharya, D. 2007 Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. Mol. Biol. Evol. 24, 1702-1713. (doi:10.1093/molbev/msm089)
75. Hagopian, J. C., Reis, M., Kitajima, J. P., Bhattacharya, D. & de Oliveira, M. C. 2004 Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui provides insights into the evolution of rhodoplasts and their relationship to other plastids. J. Mol. Evol. 59, 464-477. (doi:10.1007/s00239-004-2638- 3)
76. Hallick, R. B., Hong, L., Drager, R. G., Favreau, M. R., Monfort, A., Orsat, B., Spielmann, A. & Stutz, E. 1993 Complete sequence of Euglena gracilis chloroplast DNA. Nucl. Acids Res. 21, 3537-3544. (doi:10.1093/nar/21.15.3537)
77. Hampl, V., Hug, L., Leigh, J. W., Dacks, J. B., Lang, B. F., Simpson, A. G. & Roger, A. J. 2009 Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic 'supergroups'. Proc. Natl Acad. Sci. USA 106, 3859-3864. (doi:10.1073/pnas.0807880106)
78. Harper, J. T. & Keeling, P. J. 2003 Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol. Biol. Evol. 20, 1730-1735. (doi:10.1093/molbev/msg195)
79. Helmchen, T. A., Bhattacharya, D. & Melkonian, M. 1995 Analyses of ribosomal RNA sequences from glaucocystophyte cyanelles provide new insights into the evolutionary relationships of plastids. J. Mol. Evol. 41, 203-210.
80. Hempel, F., Bozarth, A., Sommer, M. S., Zauner, S., Przyborski, J. M. & Maier, U. G. 2007 Transport of nuclear-encoded proteins into secondarily evolved plastids. Biol. Chem. 388, 899-906. (doi:10.1515/BC.2007. 119)
81. Hibberd, D. J. & Norris, R. E. 1984 Cytology and ultrastructure of Chlorarachnion reptans (Chlorarachniophyta divisio nova, Chlorarachniophyceae classis nova). J. Phycol. 20, 310-330. (doi:10.1111/j.0022-3646.1984.00310.x)
82. Hirakawa, Y., Kofuji, R. & Ishida, K.-I. 2008 Transient transformation of a chlorarachniophyte alga, Lotharella amoebiformis (Chlorarachniophyceae), with uidA and egfp reporter genes. J. Phycol. 44, 814-820. (doi:10.1111/j.1529-8817.2008.00513.x)
83. Hjort, K., Goldberg, A. V., Tsaousis, A. D., Hirt, R. P. & Embley, T. M. 2010 Diversity and reductive evolution of mitochondria among microbial eukaryotes. Phil. Trans. R. Soc. B 365, 713-727. (doi:10.1098/rstb.2009.0224)
84. Horiguchi, T. & Takano, Y. 2006 Serial repacement of a diatom endosymbiont in the marine dinoflagellate Peridinium quinquecorne (Peridinales, Dinophyceae). Phycol. Res. 54, 193-200. (doi:10.1111/j.1440-1835.2006.00426.x)
85. Hormann, F., Soll, J. & Bolter, B. 2007 The chloroplast protein import machinery: a review. Meth. Mol. Biol. 390, 179-193. (doi:10.1007/978-1-59745-466-7-12)
86. Imanian, B. & Keeling, P. J. 2007 The dinoflagellates Durinskia baltica and Kryptoperidinium foliaceum retain functionally overlapping mitochondria from two evolutionarily distinct lineages. BMC Evol. Biol. 7, 172. (doi:10.1186/1471-2148-7-172)
87. Ishida, K., Yabuki, A. & Ota, S. 2007 The chlorarachniophytes: evolution and classification. In Unravelling the algae - the past, present, and future of algal systematics, vol. 75 (eds J. Brodie & J. Lewis). Boca Raton, FL: CRC Press.
88. Johnson, P. W., Hargraves, P. E. & Sieburth, J. M. 1988 Ultrastructure and ecology of Calycomonas ovalis Wulff, 1919, (Chrysophyceae) and its redescription as a testate rhizopod, Paulinella ovalis n. comb. (Filosea: Euglyphina). J. Protozool. 35, 618-626.
89. Kalanon, M., Tonkin, C. J. & McFadden, G. I. 2009 Characterization of two putative protein translocation components in the apicoplast of Plasmodium falciparum. Eukaryot. Cell 8, 1146-1154. (doi:10.1128/EC.00061-09)
90. Keeling, P. J. 2001 Foraminifera and Cercozoa are related in actin phylogeny: two orphans find a home? Mol. Biol. Evol. 18, 1551-1557.
91. Keeling, P. J. 2004 The diversity and evolutionary history of plastids and their hosts. Am. J. Bot. 91, 1481-1493. (doi:10.3732/ajb.91. 10.1481)
92. Keeling, P. J. 2008 Evolutionary biology: bridge over troublesome plastids. Nature 451, 896-897. (doi:10.1038/451896a)
93. Keeling, P. J. In press. Chromalveolates and the evolution of plastids by secondary endosymbiosis. J. Eukaryot. Microbiol.
94. Keeling, P. J. & Archibald, J. M. 2008 Organelle evolution: what's in a name? Curr. Biol. 18, R345-R347. (doi:10.1016/j.cub.2008.02. 065)
95. Keeling, P. J. & Palmer, J. D. 2008 Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9, 605-618. (doi:10.1038/nrg2386)
96. Keeling, P. J., Palmer, J. D., Donald, R. G., Roos, D. S., Waller, R. F. & McFadden, G. I. 1999 Shikimate pathway in apicomplexan parasites. Nature 397, 219-220. (doi:10.1038/16618)
97. Khan, H., Parks, N., Kozera, C., Curtis, B. A., Parsons, B. J., Bowman, S. & Archibald, J. M. 2007 Plastid genome sequence of the cryptophyte alga Rhodomonas salina CCMP1319: lateral transfer of putative DNA replication machinery and a test of chromist plastid phylogeny. Mol. Biol. Evol. 24, 1832-1842. (doi:10.1093/molbev/msm101)
98. Kies, L. 1974 Elektronenmikroskopische Untersuchungen an Paulinella chromatophora Lauterborn, einer Thekamöbe mit blau-grünen Endosymbionten (Cyanellen). Protoplasma 80, 69-89. (doi:10.1007/BF01666352)
99. Kies, L. & Kremer, B. P. 1979 Function of cyanelles in the Tecamoeba Paulinella chromatophora. Naturewissenschaften 66, 578-579. (doi:10.1007/BF00368819)
100. Kim, E. & Graham, L. E. 2008 EEF2 analysis challenges the monophyly of Archaeplastida and Chromalveolata. PLoS ONE 3, e2621. (doi:10.1371/journal.pone.0002621)
101. Kite, G. C., Rothschild, L. J. & Dodge, J. D. 1988 Nuclear and plastid DNAs from the binucleate dinoflagellates Glenodinium foliaceum and Peridinium balticum. Biosystems 21, 151-164. (doi:10.1016/0303-2647(88)90008-1)
102. Knauf, U. & Hachtel, W. 2002 The genes encoding subunits of ATP synthase are conserved in the reduced plastid genome of the heterotrophic alga Prototheca wickerhamii. Mol. Genet. Genom. 267, 492-497. (doi:10.1007/s00438-002-0681-6)
103. Köhler, S., Delwiche, C. F., Denny, P. W., Tilney, L. G., Webster, P., Wilson, R. J. M., Palmer, J. D. & Roos, D. S. 1997 A plastid of probable green algal origin in apicomplexan parasites. Science 275, 1485-1489. (doi:10.1126/science.275.5305.1485)
104. Kowallik, K. V. 1997 Origin and evolution of chloroplasts: current status and future perspectives. In Eukaryotism and symbiosis: intertaxonic combination versus symbiotic adaptation (eds H. E. Schenk, R. G. Herrmann, K. W. Jeon, N. E. Müller & W. Schwemmler), pp. 3-23. Berlin, Germany: Springer.
105. Krause, K. 2008 From chloroplasts to 'cryptic' plastids: evolution of plastid genomes in parasitic plants. Curr. Genet. 54, 111-121. (doi:10.1007/s00294-008-0208-8)
106. Lane, C. E., van den Heuvel, K., Kozera, C., Curtis, B. A., Parsons, B. J., Bowman, S. & Archibald, J. M. 2007 Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function. Proc. Natl Acad. Sci. USA 104, 19 908-19 913. (doi:10.1073/pnas.0707419104)
107. Leedale, G. F. 1967 Euglenoid flagellates. Englewood Cliffs, NJ: Prentice-Hall.
108. Leedale, G. F. & Vickerman, K. 2000 Phylum Euglenozoa. In An illustrated guide to the Protozoa (eds J. J. Lee, G. F. Leedale & P. Bradbury), pp. 1135-1185, 2nd edn. Lawrence, KA: Society of Protozoologists.
109. Lewis, L. A. & McCourt, R. M. 2004 Green algae and the origin of land plants. Am. J. Bot. 91, 1535-1556. (doi:10.3732/ajb.91.10.1535)
110. Lim, L. & McFadden, G. 2010 The evolution, metabolism and functions of the apicoplast. Phil. Trans. R. Soc. B 365, 749-763. (doi:10.1098/rstb.2009.0273)
111. Lithgow, T. 2000 Targeting of proteins to mitochondria. FEBS Lett. 476, 22-26. (doi:10.1016/S0014-5793(00)01663-X)
112. Ludwig, M. & Gibbs, S. P. 1989 Evidence that nucleomorphs of Chlorarachnion reptans (Chlorarachniophyceae) are vestigial nuclei: morphology, division and DNA-DAPI fluorescence. J. Phycol. 25, 385-394. (doi:10.1111/j.1529-8817.1989.tb00135.x)
113. Lukes, J., Leander, B. S. & Keeling, P. J. 2009 Cascades of convergent evolution: the corresponding evolutionary histories of euglenozoans and dinoflagellates. Proc. Natl Acad. Sci. USA 106, 9963-9970. (doi:10.1073/pnas.0901004106)
114. Maier, U. G., Rensing, S. A., Igloi, G. L. & Maerz, M. 1995 Twintrons are not unique to the Euglena chloroplast genome: structure and evolution of a plastome cpn60 gene from a cryptomonad. Mol. Gen. Genet. 246, 128-131. (doi:10.1007/BF00290141)
115. Martin,W. 1999 A briefly argued case that mitochondria and plastids are descendants of endosymbionts, but that the nuclear compartment is not. Proc. R. Soc. Lond. B 266, 1387-1395. (doi:10.1098/rspb.1999.0792)
116. Martin, W., Stoebe, B., Goremykin, V., Hansmann, S., Hasegawa, M. & Kowallik, K. V. 1998 Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393, 162-165. (doi:10.1038/30234)
117. Martin, W. et al. 2002 Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl Acad. Sci. USA 99, 12 246-12 251. (doi:10.1073/pnas.182432999)
118. Marin, B., Nowack, E. C. & Melkonian, M. 2005 A plastid in the making: evidence for a second primary endosymbiosis. Protist 156, 425-432. (doi:10.1016/j.protis.2005.09.001)
119. Matsuzaki, M., Kuroiwa, H., Kuroiwa, T., Kita, K. & Nozaki, H. 2008 A cryptic algal group unveiled: a plastid biosynthesis pathway in the oyster parasite Perkinsus marinus. Mol. Biol. Evol. 25, 1167-1179. (doi:10.1093/molbev/msn064)
120. McEwan, M. L. & Keeling, P. J. 2004 HSP90, tubulin and actin are retained in the tertiary endosymbiont genome of Kryptoperidinium foliaceum. J. Eukaryot. Microbiol. 51, 651-659. (doi:10.1111/j.1550-7408.2004. tb00604.x)
121. McFadden, G. I. 1999 Plastids and protein targeting. J. Eukaryot. Microbiol. 46, 339-346. (doi:10.1111/j.1550-7408.1999.tb04613.x)
122. McFadden, G. I. 2001 Primary and secondary endosymbiosis and the origin of plastids. J. Phycol. 37, 951-959. (doi:10.1046/j.1529-8817. 2001.01126.x)
123. McFadden, G. I. &Waller, R. F. 1997 Plastids in parasites of humans. Bioessays 19, 1033-1040. (doi:10.1002/bies.950191114)
124. McFadden, G. I., Gilson, P. R., Hofmann, C. J., Adcock, G. J. & Maier, U. G. 1994 Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga. Proc. Natl Acad. Sci. USA 91, 3690-3694. (doi:10.1073/pnas.91.9.3690)
125. McFadden, G. I., Reith, M., Munholland, J. & Lang-Unnasch, N. 1996 Plastid in human parasites. Nature 381, 482. (doi:10.1038/ 381482a0)
126. McFadden, G. I., Gilson, P. R., Douglas, S. E., Cavalier-Smith, T., Hofmann, C. J. & Maier, U. G. 1997a Bonsai genomics: sequencing the smallest eukaryotic genomes. Trends Genet. 13, 46-49. (doi:10.1016/S0168-9525(97)01010-X)
127. McFadden, G. I., Gilson, P. R. & Hofmann, C. J. B. 1997b Division Chlorarachniophyta. Origins of algae and their plastids. Wien, New York: Springer-Verlag.
128. McNeal, J. R., Kuehl, J. V., Boore, J. L. & de Pamphilis, C. W. 2007 Complete plastid genome sequences suggest strong selection for retention of photosynthetic genes in the parasitic plant genus. Cuscuta. BMC Plant Biol. 7, 57. (doi:10.1186/1471-2229-7-57)
129. Moore, R. B. et al. 2008 A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451, 959-963. (doi:10.1038/nature06635)
130. Moreira, D., Le Guyader, H. & Phillippe, H. 2000 The origin of red algae and the evolution of chloroplasts. Nature 405, 69-72. (doi:10.1038/35011054)
131. Morse, D., Salois, P., Markovic, P. & Hastings, J. W. 1995 A nuclear-encoded form II RuBisCO in dinoflagellates. Science 268, 1622-1624. (doi:10.1126/science.7777861)
132. Nakayama, T. & Ishida, K. 2009 Another acquisition of a primary photosynthetic organelle is underway in Paulinella chromatophora. Curr. Biol. 19, R284-R285. (doi:10.1016/j.cub.2009.02.043)
133. Nassoury, N., Cappadocia, M. & Morse, D. 2003 Plastid ultrastructure defines the protein import pathway in dinoflagellates. J. Cell Sci. 116, 2867-2874. (doi:10.1242/jcs.00517)
134. Nickol, A. A., Muller, N. E., Bausenwein, U., Bayer, M. G., Maier, T. L. & Schenk, H. E. 2000 Cyanophora paradoxa: nucleotide sequence and phylogeny of the nucleus encoded muroplast fructose-1,6-bisphosphate aldolase. Z. Naturforsch. 55, 991-1003.
135. Nickrent, D. L., Ouyang, Y., Duff, R. J. & dePamphilis, C. W. 1997 Do nonasterid holoparasitic flowering plants have plastid genomes? Plant Mol. Biol. 34, 717-729. (doi:10.1023/A:1005860632601)
136. Nickrent, D. L., Duff, R. J., Colwell, A. E., Wolfe, A. D., Young, N. D., Steiner, K. E. & dePamphilis, C. W. 1998 Molecular phylogenetic and evolutionary studies of parasitic plants. In Molecular systematics of plants II. DNA sequencing (eds D. E. Soltis, P. S. Soltis & J. J. Doyle), pp. 211-241. Boston, MA: Kluwer.
137. Nikolaev, S. I., Berney, C., Fahrni, J. F., Bolivar, I., Polet, S., Mylnikov, A. P., Aleshin, V. V., Petrov, N. B. & Pawlowski, J. 2004 The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proc. Natl Acad. Sci. USA 101, 8066-8071. (doi:10.1073/pnas.0308602101)
138. Nosenko, T. & Bhattacharya, D. 2007 Horizontal gene transfer in chromalveolates. BMC Evol. Biol. 7, 173. (doi:10.1186/1471-2148-7- 173)
139. Nosenko, T., Lidie, K. L., Van Dolah, F. M., Lindquist, E., Cheng, J. F. & Bhattacharya, D. 2006 Chimeric plastid proteome in the Florida 'red tide' dinoflagellate Karenia brevis. Mol. Biol. Evol. 23, 2026-2038. (doi:10.1093/molbev/msl074)
140. Not, F., Valentin, K., Romari, K., Lovejoy, C., Massana, R., Tobe, K., Vaulot, D. & Medlin, L. K. 2007 Picobiliphytes: a marine picoplanktonic algal group with unknown affinities to other eukaryotes. Science 315, 253-255. (doi:10.1126/science.1136264)
141. Nowack, E. C., Melkonian, M. & Glockner, G. 2008 Chromatophore genome sequence of Paulinella sheds light on acquisition of photosynthesis by eukaryotes. Curr. Biol. 18, 410-418. (doi:10.1016/j.cub.2008.02. 051)
142. Obornik, M. & Green, B. R. 2005 Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Mol. Biol. Evol. 22, 2343-2353. (doi:10.1093/molbev/msi230)
143. Okamoto, N. & Inouye, I. 2005 The katablepharids are a distant sister group of the Cryptophyta: a proposal for Katablepharidophyta divisio nova/Kathablepharida phylum novum based on SSU rDNA and beta-tubulin phylogeny. Protist 156, 163-179. (doi:10.1016/j.protis.2004.12.003)
144. Okamoto, N., Chantangsi, C., Horak, A., Leander, B. S. & Keeling, P. J. 2009 Molecular phylogeny and description of the novel katablepharid, Roombia truncata gen. et sp. nov., and establishment of the Hacrobia taxon nov. PLoS One e7080. (doi:10.1371/journal.pone.0007080)
145. Palmer, J. D. 1985 Comparative organization of chloroplast genomes. Annu. Rev. Genet. 19, 325-354. (doi:10.1146/annurev.ge.19.120185. 001545)
146. Palmer, J. D. 1996 Rubisco surprises in dinoflagellates. Plant Cell 8, 343-345. (doi:10.1105/tpc.8.3.343)
147. Palmer, J. D. 2003 The symbiotic birth and spread of plastids: how many times and whodunit? J. Phycol. 39, 1-9. (doi:10.1046/j.1529-8817. 2003.02185.x)
148. Park, J. M., Manen, J. F. & Schneeweiss, G. M. 2007 Horizontal gene transfer of a plastid gene in the non-photosynthetic flowering plants Orobanche and Phelipanche (Orobanchaceae). Mol. Phylogenet. Evol. 43, 974-985. (doi:10.1016/j.ympev.2006.10.011)
149. Patron, N. J. & Waller, R. F. 2007 Transit peptide diversity and divergence: a global analysis of plastid targeting signals. Bioessays 29, 1048-1058. (doi:10.1002/bies.20638)
150. Patron, N. J., Rogers, M. B. & Keeling, P. J. 2004 Gene replacement of fructose-1,6-bisphosphate aldolase (FBA) supports a single photosynthetic ancestor of chromalveolates. Eukaryot. Cell 3, 1169-1175. (doi:10.1128/EC.3.5.1169-1175.2004)
151. Patron, N. J., Waller, R. F., Archibald, J. M. & Keeling, P. J. 2005 Complex protein targeting to dinoflagellate plastids. J. Mol. Biol. 348, 1015-1024. (doi:10.1016/j.jmb.2005.03.030)
152. Patron, N. J., Waller, R. F. & Keeling, P. J. 2006 A tertiary plastid uses genes from two endosymbionts. J. Mol. Biol. 357, 1373-1382. (doi:10.1016/j.jmb.2006.01.084)
153. Patron, N. J., Inagaki, Y. & Keeling, P. J. 2007 Multiple gene phylogenies support the monophyly of cryptomonad and haptophyte host lineages. Curr. Biol. 17, 887-891. (doi:10.1016/j.cub.2007.03.069)
154. Ralph, S. A., Van Dooren, G. G., Waller, R. F., Crawford, M. J., Fraunholz, M. J., Foth, B. J., Tonkin, C. J., Roos, D. S. & McFadden, G. I. 2004 Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat. Rev. Microbiol. 2, 203-216. (doi:10.1038/nrmicro843)
155. Rensing, S. A., Goddemeier, M., Hofmann, C. J. & Maier, U. G. 1994 The presence of a nucleomorph hsp70 gene is a common feature of Cryptophyta and Chlorarachniophyta. Curr. Genet. 26, 451-455. (doi:10.1007/ BF00309933)
156. Reyes-Prieto, A., Hackett, J. D., Soares, M. B., Bonaldo, M. F. & Bhattacharya, D. 2006 Cyanobacterial contribution to algal nuclear genomes is primarily limited to plastid functions. Curr. Biol. 16, 2320-2325. (doi:10.1016/j.cub.2006.09.063)
157. Reyes-Prieto, A., Moustafa, A. & Bhattacharya, D. 2008 Multiple genes of apparent algal origin suggest ciliates may once have been photosynthetic. Curr. Biol. 18, 956-962. (doi:10.1016/j.cub.2008.05.042)
158. Rice, D. W. & Palmer, J. D. 2006 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.
159. Richardson, A. O. & Palmer, J. D. 2007 Horizontal gene transfer in plants. J. Exp. Bot. 58, 1-9. (doi:10.1093/jxb/erl148)
160. Roberts, F. et al. 1998 Evidence for the shikimate pathway in apicomplexan parasites. Nature 393, 801-805. (doi:10.1038/30718)
161. Rodriguez-Ezpeleta, N., Brinkmann, H., Burey, S. C., Roure, B., Burger, G., Loffelhardt, W., Bohnert, H. J., Philippe, H. & Lang, B. F. 2005 Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr. Biol. 15, 1325-1330. (doi:10.1016/j.cub.2005. 06.040)
162. Rogers, M. B. & Keeling, P. J. 2003 Lateral gene transfer and re-compartmentalisation of Calvin cycle enzymes in plants and algae. J. Mol. Evol. 58, 367-375. (doi:10.1007/s00239-003-2558-7)
163. Rogers, M. B., Gilson, P. R., Su, V., McFadden, G. I. & Keeling, P. J. 2007a The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of chlorarachniophyte and euglenid secondary endosymbionts. Mol. Biol. Evol. 24, 54-62. (doi:10.1093/molbev/msl129)
164. Rogers, M. B., Watkins, R. F., Harper, J. T., Durnford, D. G., Gray, M. W. & Keeling, P. J. 2007b A complex and punctate distribution of three eukaryotic genes derived by lateral gene transfer. BMC Evol. Biol. 7, 89. (doi:10.1186/1471-2148-7-89)
165. Rumpho, M. E., Worful, J. M., Lee, J., Kannan, K., Tyler, M. S., Bhattacharya, D., Moustafa, A. & Manhart, J. R. 2008 Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc. Natl Acad. Sci. USA 105, 17 867-17 871. (doi:10.1073/pnas.0804968105)
166. Saldarriaga, J. F., Taylor, F. J. R., Keeling, P. J. & Cavalier-Smith, T. 2001 Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J. Mol. Evol. 53, 204-213. (doi:10.1007/s002390010210)
167. Sato, S., Clough, B., Coates, L. & Wilson, R. J. 2004 Enzymes for heme biosynthesis are found in both the mitochondrion and plastid of the malaria parasite Plasmodium falciparum. Protist 155, 117-125. (doi:10.1078/1434461000169)
168. Schnepf, E. & Deichgraber, G. 1984 'Myzocytosis,' a kind of endocytosis with implications to compartmentalization in endosymbiosis. Naturwissenschaften 71, 218-219. (doi:10.1007/BF00490442)
169. Schnepf, E. & Elbrächter, M. 1988 Cryptophycean-like double membrane-bound chloroplast in the dinoflagellate, Dinophysis Ehrenb.: evolutionary, phylogenetic and toxicological implications. Bot. Acta. 101, 196-203.
170. Sekiguchi, H., Moriya, M., Nakayama, T. & Inouye, I. 2002 Vestigial chloroplasts in heterotrophic stramenopiles Pteridomonas danica and Ciliophrys infusionum (Dictyochophyceae). Protist 153, 157-167. (doi:10.1078/1434-4610-00094)
171. Sepsenwol, S. 1973 Leucoplast of the cryptomonad Chilomonas paramecium. Evidence for presence of a true plastid in a colorless flagellate. Exp. Cell Res. 76, 395-409. (doi:10.1016/0014-4827(73) 90392-3)
172. Sheveleva, E. V. & Hallick, R. B. 2004 Recent horizontal intron transfer to a chloroplast genome. Nucl. Acids Res. 32, 803-810. (doi:10.1093/nar/gkh225)
173. Silver, T. D., Koike, S., Yabuki, A., Kofuji, R., Archibald, J. M. & Ishida, K. 2007 Phylogeny and nucleomorph karyotype diversity of chlorarachniophyte algae. J. Eukaryot. Microbiol. 54, 403-410. (doi:10.1111/j.1550-7408.2007.00279.x)
174. Siu, C., Swift, H. & Chiang, K. 1976 Characterization of cytoplasmic and nuclear genomes in the colorless alga Polytoma. I. Ultrastructural analysis of organelles. J. Cell. Biol. 69, 352-370. (doi:10.1083/jcb.69.2.352)
175. Slamovits, C. H. & Keeling, P. J. 2008 Plastid-derived genes in the nonphotosynthetic alveolate Oxyrrhis marina. Mol. Biol. Evol. 25, 1297-1306. (doi:10.1093/molbev/msn075)
176. Slamovits, C. H. & Keeling, P. J. 2009 Evolution of ultrasmall spliceosomal introns in highly reduced nuclear genomes. Mol. Biol. Evol. 26, 1699-1705. (doi:10.1093/molbev/msp081)
177. Sommer, M. S., Gould, S. B., Lehmann, P., Gruber, A., Przyborski, J. M. & Maier, U. G. 2007 Der1-mediated preprotein import into the periplastid compartment of chromalveolates? Mol. Biol. Evol. 24, 918-928. (doi:10.1093/molbev/msm008)
178. Steiner, J. M. & Loffelhardt, W. 2002 Protein import into cyanelles. Trends Plant Sci. 7, 72-77. (doi:10.1016/S1360-1385(01)02179-3)
179. Stelter, K., El-Sayed, N. M. & Seeber, F. 2007 The expression of a plant-type ferredoxin redox system provides molecular evidence for a plastid in the early dinoflagellate Perkinsus marinus. Protist 158, 119-130. (doi:10.1016/j.protis.2006.09.003)
180. Stiller, J. W., Riley, J. & Hall, B. D. 2001 Are red algae plants? A critical evaluation of three key molecular data sets. J. Mol. Evol. 52, 527-539.
181. Stiller, J. W., Reel, D. C. & Johnson, J. C. 2003 A single origin of plastids revisited: convergent evolution in organellar genome content. J. Phycol. 39, 95-105. (doi:10.1046/j.1529-8817.2003.02070.x)
182. Stoebe, B. & Maier, U. G. 2002 One, two, three: nature's tool box for building plastids. Protoplasma 219, 123-130. (doi:10.1007/ s007090200013)
183. Sulli, C., Fang, Z., Muchhal, U. & Schwartzbach, S. D. 1999 Topology of Euglena chloroplast protein precursors within endoplasmic reticulum to Golgi to chloroplast transport vesicles. J. Biol. Chem. 274, 457-463. (doi:10.1074/jbc.274.1.457)
184. Takano, Y., Hansen, G., Fujita, D. & Horiguchi, T. 2008 Serial replacement of diatom endosymbiont in two freshwater dinoflagellates, Peridiniopsis spp. (Peridiniales, Dinophyceae). Phycologia 47, 41-53. (doi:10.2216/07-36.1)
185. Tartar, A., Boucias, D. G., Adams, B. J. & Becnel, J. J. 2002 Phylogenetic analysis identifies the invertebrate pathogen Helicosporidium sp. as a green alga (Chlorophyta). Int. J. Syst. Evol. Microbiol. 52, 273-279.
186. Tartar, A., Boucias, D. G., Adams, B. J. & Becnel, J. J. 2003 Comparison of plastid 16S rDNA (rrn16) from Helicosporidium spp.: evidence supporting the reclassification of Helicosporidia as green algae (Chlorophyta). Int. J. Syst. Evol. Microbiol. 53, 1719-1723. (doi:10.1099/ijs.0.02559-0)
187. Teles-Grilo, M. L., Tato-Costa, J., Duarte, S. M., Maia, A., Casal, G. & Azevedo, C. 2007 Is there a plastid in Perkinsus atlanticus (Phylum Perkinsozoa)? Eur. J. Protistol. 43, 163-167. (doi:10.1016/j.ejop. 2007.02.002)
188. Tengs, T., Dahlberg, O. J., Shalchian-Tabrizi, K., Klaveness, D., Rudi, K., Delwiche, C. F. & Jakobsen, K. S. 2000 Phylogenetic analyses indicate that the 19′hexanoyloxyfucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Mol. Biol. Evol. 17, 718-729.
189. Theissen, U. & Martin, W. 2006 The difference between organelles and endosymbionts. Curr. Biol. 16, R1016-R1017. Author reply R1017-8. (doi:10.1016/j.cub.2006.11.020)
190. Turmel, M., Gagnon, M. C., O'Kelly, C. J., Otis, C. & Lemieux, C. 2009 The chloroplast genomes of the green algae Pyramimonas, Monomastix, and Pycnococcus shed new light on the evolutionary history of prasinophytes and the origin of the secondary chloroplasts of euglenids. Mol. Biol. Evol. 26, 631-648. (doi:10.1093/molbev/msn285)
191. Turner, S., Pryer, K. M., Miao, V. P. & Palmer, J. D. 1999 Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J. Eukaryot. Microbiol. 46, 327-338. (doi:10.1111/j.1550-7408.1999.tb04612.x)
192. Tyler, B. M. et al. 2006 Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313, 1261-1266. (doi:10.1126/science.1128796)
193. Valentin, K. & Zetsche, K. 1989 The genes of both subunits of ribulose-1,5-bisphosphate carboxylase constitute an operon on the plastome of a red alga. Curr. Genet. 16, 203-209. (doi:10.1007/BF00391478)
194. van der Giezen, M., Tovar, J. & Clark, C. G. 2005 Mitochondrion-derived organelles in protists and fungi. Int. Rev. Cytol. 244, 175-225.
195. van Dooren, G. G., Schwartzbach, S. D., Osafune, T. & McFadden, G. I. 2001 Translocation of proteins across the multiple membranes of complex plastids. Biochim. Biophys. Acta 1541, 34-53. (doi:10.1016/S0167- 4889(01)00154-9)
196. Waller, R. F., Keeling, P. J., van Dooren, G. G. & McFadden, G. I. 2003 Comment on 'A green algal apicoplast ancestor'. Science 301, 49. (doi:10.1126/science.1083647)
197. Waller, R. F., Patron, N. J. & Keeling, P. J. 2006a Phylogenetic history of plastid-targeted proteins in the peridinin-containing dinoflagellate Heterocapsa triquetra. Int. J. Syst. Evol. Microbiol. 56, 1439-1447. (doi:10.1099/ijs.0.64061-0)
198. Waller, R. F., Slamovits, C. H. & Keeling, P. J. 2006b Lateral gene transfer of a multigene region from cyanobacteria to dinoflagellates resulting in a novel plastid-targeted fusion protein. Mol. Biol. Evol. 23, 1437-1443. (doi:10.1093/molbev/msl008)
199. Watanabe, M. M., Suda, S., Inouye, I., Sawaguchi, I. & Chihara, M. 1990 Lepidodinium viride gen et sp. nov. (Gymnodiniales, Dinophyta), a green dinoflagellate with a chlorophyll a- and b-containing endosymbiont. J. Phycol. 26, 741-751. (doi:10.1111/j.0022-3646. 1990.00741.x)
200. Whatley, J. M., John, P. & Whatley, F. R. 1979 From extracellular to intracellular: the establishment of mitochondria and chloroplasts. Proc. R. Soc. Lond. B 204, 165-187. (doi:10.1098/rspb.1979.0020)
201. Whitney, S. M., Shaw, D. C. & Yellowlees, D. 1995 Evidence that some dinoflagellates contain a ribulose-1,5-bisphosphate carboxylase/oxygenase related to that of the alpha-proteobacteria. Proc. R. Soc. Lond. B 259, 271-275. (doi:10.1098/rspb.1995.0040)
202. Wickner, W. & Schekman, R. 2005 Protein translocation across biological membranes. Science 310, 1452-1456. (doi:10.1126/ science.1113752)
203. Williams, B. A. & Hirt, R. P. 2004 RACE and RAGE cloning in parasitic microbial eukaryotes. Meth. Mol. Biol. 270, 151-172.
204. Williams, B. A. P. & Keeling, P. J. 2003 Cryptic organelles in parasitic protists and fungi. Adv. Parasitol. 54, 9-67. (doi:10.1016/S0065-308X(03)54001-5)
205. Williams, B. A. P., Slamovits, C. H., Patron, N. J., Fast, N. M. & Keeling, P. J. 2005 A high frequency of overlapping gene expression in compacted eukaryotic genomes. Proc. Natl Acad. Sci. USA 102, 10 936-10 941. (doi:10.1073/pnas.0501321102)
206. Williamson, D. H., Gardner, M. J., Preiser, P., Moore, D. J., Rangachari, K. & Wilson, R. J. 1994 The evolutionary origin of the 35 kb circular DNA of Plasmodium falciparum: new evidence supports a possible rhodophyte ancestry. Mol. Gen. Genet. 243, 249-252.
207. Wilson, R. J. 2002 Progress with parasite plastids. J. Mol. Biol. 319, 257-274. (doi:10.1016/S0022-2836(02)00303-0)
208. Wilson, R. J. M. I. et al. 1996 Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 261, 155-172. (doi:10.1006/jmbi.1996.0449)
209. Wolfe, A. D. & dePamphilis, C. W. 1997 Alternate paths of evolution for the photosynthetic gene rbcL in four non-photosynthetic species of Orobanche. Plant Mol. Biol. 33, 965-977. (doi:10.1023/A: 1005739223993)
210. Wolfe, G. R., Cunningham, F. X., Durnford, D. G., Green, B. R. & Gantt, E. 1995 Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 367, 566-568. (doi:10.1038/367566a0)
211. Xu, P. et al. 2004 The genome of Cryptosporidium hominis. Nature 431, 1107-1112. (doi:10.1038/nature02977)
212. Yoon, H. S., Hackett, J. D., Pinto, G. & Bhattacharya, D. 2002 A single, ancient origin of the plastid in the Chromista. Proc. Natl Acad. Sci. USA 99, 15 507-15 512. (doi:10.1073/pnas.242379899)
213. Yoon, H. S., Reyes-Prieto, A., Melkonian, M. & Bhattacharya, D. 2006 Minimal plastid genome evolution in the Paulinella endosymbiont. Curr. Biol. 16, R670-R672. (doi:10.1016/j.cub.2006.08.018)