Transcriptomic analysis reveals evidence for a cryptic plastid in the colpodellid Voromonas pontica, a close relative of chromerids and apicomplexan parasites

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Gile, Gillian H ^a   Slamovits, Claudio H ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; HEME; IRON; ISOPRENOID; PHOSPHATE TRANSPORTER; SMALL SUBUNIT RIBOSOMAL RNA; SULFUR; TETRAPYRROLE DERIVATIVE; TRANSCRIPTOME;

APICOMPLEXA; APICOPLAST; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; FLAGELLATE; GENE CLUSTER; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN TARGETING; RNA SEQUENCE; SEQUENCE HOMOLOGY; TRANSCRIPTOMICS; UNINDEXED SEQUENCE; VOROMONAS PONTICA; ALVEOLATA; EVOLUTION; GENE EXPRESSION PROFILING; GENETICS; PHYSIOLOGY; PLASTID; ULTRASTRUCTURE;

ALVEOLATA; BIOLOGICAL EVOLUTION; GENE EXPRESSION PROFILING; PHYLOGENY; PLASTIDS; TRANSCRIPTOME;

EID: 84900402320     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096258     Document Type: Article

References (127)

1. Wolfe KH, Morden CW, Palmer JD (1992) Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci U S A 89: 10648-10652.
2. Wickett NJ, Zhang Y, Hansen SK, Roper JM, Kuehl JV, et al. (2008) Functional gene losses occur with minimal size reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Mol Biol Evol 25: 393-401. (Pubitemid 351231612)
3. Round FE (1980) The evolution of pigmented and unpigmented unicells: a consideration of the protista. Biosystems 12: 61-69.
4. Rumpf R, Vernon D, Schreiber D, Birky CW (1996) Evolutionary consequences of the loss of photosynthesis in Chlamydomonadaceae: phylogenetic analysis of Rrn18 (18S rDNA) in 13 Polytoma strains (Chlorophyta). J Phycol 32: 119-126.
5. Tartar A, Boucias DG, Becnel JJ, Adams BJ (2003) Comparison of plastid 16S rRNA (rrn16) genes from Helicosporidium spp.: evidence supporting the reclassification of Helicosporidia as green algae (Chlorophyta). Int J Syst Evol Microbiol 53: 1719-1723. (Pubitemid 37483827)
6. Borza T, Popescu CE, Lee RW (2005) Multiple metabolic roles for the nonphotosynthetic plastid of the green alga Prototheca wickerhamii. Eukaryotic Cell 4: 253-261. (Pubitemid 40257125)
7. Blouin NA, Lane CE (2012) Red algal parasites: models for a life history evolution that leaves photosynthesis behind again and again. Bioessays 34: 226-235.
8. Hoef-Emden K (2005) Multiple independent losses of photosynthesis and differing evolutionary rates in the genus Cryptomonas (Cryptophyceae): combined phylogenetic analyses of DNA sequences of the nuclear and nucleomorph ribosomal operons. J Mol Evol 60: 183-195.
9. Marin B, Palm A, Klingberg M, Melkonian M (2003) Phylogeny and taxonomic revision of plastid-containing euglenophytes based on SSU rDNA sequence comparisons and synapomorphic signatures in the SSU rRNA secondary structure. Protist 154: 99-145. (Pubitemid 36689243)
10. Thomsen HA, Bjørn PDP, Højlund L, Olesen J, Pedersen JB (1995) Ericiolus gen. nov. (Prymnesiophyceae), a new coccolithophorid genus from polar and temperate regions. Eur. J Phycol 30: 29-34.
11. Sekiguchi H, Moriya M, Nakayama T, Inouye I (2002) Vestigial chloroplasts in heterotrophic stramenopiles Pteridomonas danica and Ciliophrys infusionum (Dictyochophyceae). Protist 153: 157-167. (Pubitemid 34674227)
12. Douzery EJP, Snell EA, Bapteste E, Delsuc F, Philippe H (2004) The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils? Proc Natl Acad Sci U S A 101: 15386-15391. (Pubitemid 39441551)
13. Parfrey LW, Lahr DJG, Knoll AH, Katz LA (2011) Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci U S A 108: 13624-13629.
14. Janouškovec J, Horák A, Oborník M, Lukeš J, Keeling PJ (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci U S A 107: 10949-10954.
15. Saldarriaga JF, Taylor FJR, Keeling PJ, Cavalier-Smith T (2001) Dinoflagellate nuclear SSU phylogeny suggests multiple plastid losses and replacements. J Mol Evol 53: 204-213. (Pubitemid 32783795)
16. Funes S, Davidson E, Reyes-Prieto A, Magallón S, Herion P, et al. (2002) A green algal apicoplast ancestor. Science 298: 2155. (Pubitemid 35471234)
17. Waller RF, Keeling PJ, van Dooren GG, McFadden GI (2003) Comment on "A green algal apicoplast ancestor". Science 301: 49a.
18. Moore RB, Oborník M, Janouškovec J, Chrudimský T, Vancová M, et al. (2008) A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451: 959-963. (Pubitemid 351301735)
19. Oborník M, Modrý D, Lukeš M, Černotí ková-Stříbrná E, Cihlář J, et al. (2012) Morphology, ultrastructure and life cycle of Vitrella brassicaformis n. sp., n. gen., a novel chromerid from the Great Barrier Reef. Protist 163: 306-323.
20. Slamovits CH, Keeling PJ (2008) Plastid-derived genes in the nonphotosynthetic alveolate Oxyrrhis marina. Mol Biol Evol 25: 1297-1306. (Pubitemid 351882005)
21. 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.
22. Carreno RA, Martin DS, Barta JR (1999) Cryptosporidium is more closely related to the gregarines than to coccidia as shown by phylogenetic analysis of apicomplexan parasites inferred using small-subunit ribosomal RNA gene sequences. Parasitol Res 85: 899-904. (Pubitemid 29467940)
23. Leander BS, Lloyd SAJ, Marshall W, Landers SC (2006) Phylogeny of marine gregarines (Apicomplexa) - Pterospora, Lithocystis, and Lankesteria - and the origin(s) of coelomic parasitism. Protist 157: 45-60. (Pubitemid 43220716)
24. Zhu G, Marchewka MJ, Keithly JS (2000) Cryptosporidium parvum appears to lack a plastid genome. Microbiol 146: 315-321. (Pubitemid 30099206)
25. Toso MA, Omoto CK (2007) Gregarina niphandrodes may lack both a plastid genome and organelle. J Eukaryotic Microbiol 54: 66-72.
26. Barta JR, Thompson RCA (2006) What is Cryptosporidium? Reappraising its biology and phylogenetic affinities. Trends Parasitol 22: 463-468. (Pubitemid 44333284)
27. Simpson AGB, Patterson DJ (1996) Ultrastructure and identification of the predatory flagellate Colpodella pugnax Cienkowski (Apicomplexa) with a description of Colpodella turpis n. sp. and a review of the genus. Syst Parasitol 33: 187-198. (Pubitemid 126709540)
28. Mylnikov AP (2000) The new marine carnivorous flagellate Colpodella pontica (Colpodellida, Protozoa). Zoologicheskiy Zhurnal 79: 261-266 (in Russian).
29. Brugerolle G (2002) Colpodella vorax: ultrastructure, predation, life-cycle, mitosis, and phylogenetic relationships. Eur J Protistol 38: 113-125.
30. Cavalier-Smith T, Chao EE (2004) Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.). Eur J Protistol 40: 185-212. (Pubitemid 39098747)
31. Brugerolle G, Mignot JP (1979) Observations sur le cycle l'ultrastructure et la position systématique de Sporomonas perforans (Bodo perforans Hollande 1938), flagellé parasite de Chilomonas paramecium: Ses relations avec les dinoflgellés et sporozoaires. Protistologica 15: 183-196.
32. Foissner W, Foissner I (1984) First record of an ectoparasitic flagellate on ciliates: an ultrastructural investigation of the morphology and the mode of attachment of Spiromonas gonderi nov. spec. (Zoomastigophora, Spiromonadidae) invading the pellicle of ciliates of the genus Colpoda (Ciliophora, Colpodidae). Protistologica 20: 635-648.
33. Kuvardina ON, Leander BS, Aleshin VV, Mylnikov AP, Keeling PJ, et al. (2002) The phylogeny of colpodellids (Alveolata) using small subunit rRNA gene sequences suggests they are the free-living sister group to apicomplexans. J Eukaryotic Microbiol 49: 498-504. (Pubitemid 36003254)
34. Leander BS, Kuvardina ON, Aleshin VV, Mylnikov AP, Keeling PJ (2003) Molecular phylogeny and surface morphology of Colpodella edax (Alveolata): insights into the phagotrophic ancestry of apicomplexans. J Eukaryotic Microbiol 50: 334-340. (Pubitemid 37144038)
35. Ralph SA, van Dooren GG, Waller RF, Crawford MJ, Fraunholz MJ, et al. (2004) Metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2: 203-216. (Pubitemid 39490083)
36. Lim L, McFadden GI (2010) The evolution, metabolism, and functions of the apicoplast. Phil Trans R Soc B 365: 749-763.
37. Seeber F, Soldati-Favre D (2010) Metabolic pathways in the apicoplast of apicomplexa. Int Rev Cell Mol Biol 281: 162-211.
38. Bispo NA, Culleton R, Silva LA, Cravo P (2013) A systematic in silico search for target similarity identifies several approved drugs with potential activity against the Plasmodium falciparum apicoplast. PLoS ONE 8: e59288.
39. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, et al. (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29: 644-652.
40. Parra G, Bradnam K, Korf I (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23: 1061-1067. (Pubitemid 47050556)
41. Parra G, Bradnam K, Ning Z, Keane T, Korf I (2009) Assessing the gene space in draft genomes. Nucleic Acids Res 37: 289-298.
42. Yuan CL, Keeling PJ, Krause PJ, Horak A, Bent S, et al. (2012) Colpodella sp.-like parasite infection in woman, China. Emerging Infect Dis 18: 125-127.
43. Bruce BD (2001) The paradox of plant transit peptides: conservation of function despite divergence in primary structure. Biochim Biophys Acta 1541: 2-21.
44. Patron NJ, Waller RF (2007) Transit peptide diversity and divergence: a global analysis of plastid targeting signals. BioEssays 29: 1048-1058. (Pubitemid 47522845)
45. Foth BJ, Ralph SA, Tonkin CJ, Struck NS, Fraunholz M, et al. (2003) Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299: 705-708. (Pubitemid 36159484)
46. Ralph SA, Foth BJ, Hall N, McFadden GI (2004) Evolutionary pressures on apicoplast transit peptides. Mol Biol Evol 21: 2183-2194. (Pubitemid 39488890)
47. Lim L, Linka M, Mullin KA, Weber APM, McFadden GI (2010) The carbon and energy sources of the non-photosynthetic plastid in the malaria parasite. FEBS Lett 584: 549-554.
48. Karnataki A, DeRocher A, Coppens I, Nash C, Feagin JE, Parsons M (2007) Cell cycle-regulated vesicular trafficking of Toxoplasma APT1, a protein localized to multiple apicoplast membranes. Mol Microbiol 63: 1653-1668. (Pubitemid 46437132)
49. Woehle C, Dagan T, Martin WF, Gould SB (2011) Red and problematic green phylogenetic signals among thousands of nuclear genes from the photosynthetic and Apicomplexa-related Chromera velia. Genome Biol Evol 3: 1220-1230.
50. Bachvaroff TR, Gornik SG, Concepcion GT, Waller RF, Mendez GS, et al. (2014) Dinoflagellate phylogeny revisited: Using ribosomal proteins to resolve deep branching dinoflagellate clades. Mol Phylogen Evol 70: 314-322.
51. Heath TA, Hedtke SM, Hillis DM (2008) Taxon sampling and the accuracy of phylogenetic analyses. J Syst Evol 46: 239-257.
52. Hedtke SM, Townsend TM, Hillis DM (2006) Resolution of phylogenetic conflict in large data sets by increased taxon sampling. Syst Biol 55: 522-529.
53. Dellibovi-Ragheb TA, Gisselberg JE, Prigge ST (2013) Parasites FeS up: iron-sulfur biogenesis in eukaryotic pathogens. PLoS Pathog 9: e1003227.
54. Xu XM, Møller SG (2011) Iron-sulfur clusters: biogenesis, molecular mechanisms, and their functional significance. Antioxid Redox Signalling 15: 271-307.
55. Lill R (2009) Function and biogenesis of iron-sulphur proteins. Nature 460: 831-838.
56. Lill R, Mühlenhoff U (2006) Iron-sulfur protein biogenesis in eukaryotes: components and mechanisms. Annu Rev Cell Dev Biol 22: 457-486.
57. Seeber F (2002) Biogenesis of iron-sulphur clusters in amitochondriate and apicomplexan protists. Int J Parasitol 32: 1207-1217.
58. van Dooren GG, Stimmler LM, McFadden GI (2006) Metabolic maps and functions of the Plasmodium mitochondrion. FEMSMicrobiol Rev. 30: 596-630. (Pubitemid 43855768)
59. Gisselberg JE, Dellibovi-Ragheb TA, Matthews KA, Bosch G, Prigge ST (2013) The Suf iron-sulfur cluster synthesis pathway is required for apicoplast maintenance in malaria parasites. PLoS Pathog 9: e1003655.
60. Butterfield ER, Howe CJ, Nisbet RER (2013) An analysis of dinoflagellate metabolism using EST data. Protist 164: 218-236.
61. Laatsch T, Zauner S, Stoebe-Maier B, Kowallik KV, Maier U-G (2004) Plastid-derived single gene minicircles of the dinoflagellate Ceratium horridum are localized in the nucleus. Mol Biol Evol 21: 1318-1322. (Pubitemid 38823734)
62. Balk J, Pilon M (2011) Ancient and essential: the assembly of iron-sulfur clusters in plants. Trends Plant Sci 16: 218-226.
63. Ellis KES, Clough B, Saldanha JW, Wilson RJM (2001) Nifs and Sufs in malaria. Mol Microbiol 41: 973-981. (Pubitemid 36124696)
64. Khan H, Parks N, Kozera C, Curtis BA, Parsons BJ, et al. (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. (Pubitemid 47236701)
65. Oudot-Le Secq M-P, Grimwood J, Shapiro H, Armbrust EV, Bowler C, Green BR (2007) Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana : comparison with other plastid genomes of the red lineage. Mol Genet Genomics 277: 427-439. (Pubitemid 46452269)
66. Donaher N, Tanifuji G, Onodera NT, Malfatti SA, Chain PSG, et al. (2009) The complete plastid genome sequence of the secondarily nonphotosynthetic alga Cryptomonas paramecium: reduction, compaction, and accelerated evolutionary rate. Genome Biol Evol 1: 439-448.
67. Wilson RJM, Denny PW, Preiser PR, Rangachari K, Roberts K, et al. (1996) Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol 261: 155-172. (Pubitemid 26275799)
68. Denny PW, Preiser PR, Williamson DH, Wilson RJM (1998) Evidence for a single origin of the 35 kbp plastid DNA in apicomplexans. Protist 149: 51-59.
69. Sanchez-Puerta MV, Bachvaroff TR, Delwiche CF (2005) The complete plastid genome sequence of the haptophyte Emiliania huxleyi: a comparison to other plastid genomes. DNA Res 12: 151-156. (Pubitemid 41321159)
70. Ong HC, Wilhelm SW, Gobler CJ, Bullerjahn G, Jacobs MA, et al. (2010) Analysis of the complete chloroplast genome sequences of two members of the Pelagophyceae: Aureococcus anophagefferens CCMP1984 and Aureoumbra lagunensis CCMP1507. J Phycol 46: 602-615.
71. Arisue N, Hashimoto T, Mitsui H, Palacpac NMQ, Kaneko A, et al. (2012) The Plasmodium apicoplast genome: conserved structure and close relationship of P. ovale to rodent malaria parasites. Mol Biol Evol 29: 2095-2099.
72. + reductase and ferredoxin. J Biol Chem 276: 5483-5490.
73. Kumar B, Chaubey S, Shah P, Tanveer A, Charan M, et al. (2011) Interaction between sulfur mobilisation proteins SufB and SufC: evidence for an iron-sulphur cluster biogenesis pathway in the apicoplast of Plasmodium falciparum. Int J Parasitol 41: 991-999.
74. Sheiner L, Demerly JL, Poulsen N, Beatty WL, Lucas O, et al. (2011) A systematic screen to discover and analyze apicoplast proteins identifies a conserved and essential protein import factor. PLoS Pathog 7: e1002392.
75. Haussig JM, Matuschewski K, Kooij TWA (2013) Experimental genetics of Plasmodium berghei NFU in the apicoplast iron-sulfur cluster biogenesis pathway. PLoS ONE 8: e67269.
76. Mihara H, Esaki N (2002) Bacterial cysteine desulfurases: their function and mechanisms. Appl Microbiol Biotechnol 60: 12-23.
77. Eisenreich W, Schwartz M, Cartayrade A, Arigoni D, Zenk MH, Bacher A (1998) The deoxyxylulose phosphate pathway of terpenoid biosynthesis in plants and microorganisms. Chem Biol 5: 221-233.
78. Gräwert T, Groll M, Rohdich F, Bacher A, Eisenreich W (2011) Biochemistry of the non-mevalonate isoprenoid pathway. Cell Mol Life Sci 68: 3797-3814.
79. Boucher Y, Doolittle WF (2000) The role of lateral transfer in the evolution of isoprenoid biosynthesis pathways. Mol Microbiol 37: 703-716. (Pubitemid 30618134)
80. Lange BM, Rujan T, Martin W, Croteau R (2000) Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc Natl Acad Sci U S A 97: 13172-13177.
81. Ralph SA, D'Ombrain MC, McFadden GI (2001) The apicoplast as an antimalarial drug target. Drug Resist Updates 4: 145-151. (Pubitemid 33089452)
82. Tonkin CJ, van Dooren GG, Spurck TP, Struck NS, Good RT, et al. (2004) Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol Biochem Parasitol 137: 13-21. (Pubitemid 38987938)
83. Baumeister S, Weisner J, Reichenberg A, Hintz M, Bietz S, et al. (2011) Fosmidomycin uptake into Plasmodium and Babesia-infected erythrocytes is facilitated by parasite-induced new permeability pathways. PLoS ONE 6: e19334.
84. Nair SC, Brooks CF, Goodman CD, Sturm A, McFadden GI, et al. (2011) Apicoplast isoprenoid precursor synthesis and the molecular basis of fosmidomycin resistance in Toxoplasma gondii. J Exp Med 208: 1547-1559.
85. Jomaa H, Wiesner J, Sanderbrande S, Altincicek B, Weidemeyer C, et al. (1999) Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285: 1573-1576. (Pubitemid 29420582)
86. Yeh E, DeRisi JL (2011) Chemical rescue of malaria parasites lacking an apicoplast defines organelle function in blood-stage Plasmodium falciparum. PLoS Biol 9: e1001138.
87. Disch A, Schwender J, Mü ller C, Lichtenthaler HK, Rohmer M (1998) Distribution of the mevalonate and glyceraldehyde phosphate/pyruvate pathways for isoprenoid biosynthesis in unicellular algae and the cyanobacterium Synechocystis PCC 6714. Biochem J 333: 381-388. (Pubitemid 28379540)
88. de Koning AP and Keeling PJ (2004) Nucleus-encoded genes for plastid-targeted proteins in Helicosporidium : functional diversity of a cryptic plastid in a parasitic alga. Eukaryotic Cell 3: 1198-1205.
89. Grauvogel C, Reece KS, Brinkmann H, Petersen J (2007) Plastid isoprene metabolism in the oyster parasite Perkinsus marinus connects dinoflagellates and malaria pathogens - new impetus for studying alveolates. J Mol Evol 65: 725-729.
90. Sanchez-Puerta MV, Lippmeier JC, Apt KE, Delwiche CF (2007) Plastid genes in a non-photosynthetic dinoflagellate. Protist 158: 105-117. (Pubitemid 44969625)
91. Xu P, Widmer G, Wang Y, Ozaki LS, Alvez JM, et al. (2004) The genome of Cryptosporidium hominis. Nature 431: 1107-1112. (Pubitemid 39472235)
92. Panek H, O'Brian MR (2002) A whole genome view of prokaryotic haem biosynthesis. Microbiol 148: 2273-2282.
93. Kořený L, Oborník M, Lukeš J (2013) Make it, take it, or leave it: heme metabolism of parasites. PLoS Pathog 9: e1003088.
94. Oborník M, Green BR (2005) Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Mol Biol Evol 22: 2343-2353. (Pubitemid 41661373)
95. Kořený L, Sobotka R, Janoušcovec J, Keeling PJ, Oborník M (2011) Tetrapyrrole synthesis of photosynthetic chromerids is likely homologous to the unusual pathway of apicomplexan parasites. Plant Cell 23: 3454-3462.
96. Weinstein JD, Beale SI (1983) Separate physiological roles and subcellular compartments for two tetrapyrrole biosynthetic pathways in Euglena gracilis. J Biol Chem 258: 6799-6807.
97. Iida K, Mimura I, Kajiwara M (2002) Evaluation of two biosynthetic pathways to d-aminolevulinic acid in Euglena gracilis. Eur J Biochem 269: 291-297. (Pubitemid 34107363)
98. Kivic PA, Vesk M (1974) An electron microscope search for plastids in bleached Euglena gracilis and in Astasia longa. Can J Bot 52: 695-699.
99. Kořený L, Oborník M (2011) Sequence evidence for the presence of two tetrapyrrole pathways in Euglena gracilis. Genome Biol Evol 3: 359-364.
100. Wu B (2006) Heme biosynthetic pathway in apicomplexan parasites. PhD dissertation (Philadelphia, PA: University of Pennsylvania).
101. Rao A, Yeleswarapu SJ, Srinivasan R, Bulusu G (2008) Localization of heme biosynthesis pathway enzymes in Plasmodium falciparum. Indian J Biochem Biophys 45: 365-373.
102. Fernández Robledo JA, Caler E, Matsuzaki M, Keeling PJ, Shanmugam D, et al. (2011) The search for the missing link: a relic plastid in Perkinsus? Int J Parasitol 41: 1217-1229.
103. Gschloessl B, Guermeur Y, Cock JM (2008) HECTAR: a method to predict subcellular targeting in heterokonts. BMC Bioinf 9: e393.
104. Tardif M, Atteia A, Specht M, Cogne G, Rolland R, et al. (2012) PredAlgo: A new subcellular localization prediction tool dedicated to green algae. Mol Biol Evol 29: 3625-3639.
105. Flügge U-I (1999) Phosphate transporters in plastids. Annu Rev Plant Physiol Plant Mol Biol 50: 27-45.
106. Weber APM, Linka M, Bhattacharya D (2006) Single, ancient origin of a plastid metabolite translocator family in Plantae from an endomembrane-derived ancestor. Eukaryotic Cell 5: 609-612.
107. Tyra HM, Linka M, Weber APM, Bhattacharya D (2008) Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol 8: R212.
108. Colleoni C, Linka M, Deschamps P, Handford MG, Dupree P, et al. (2010) Phylogenetic and biochemical evidence supports the recruitment of an ADP-glucose translocator for the export of photosynthate during plastid endosymbiosis. Mol Biol Evol 27: 2691-2701.
109. Linka M, Jamai A, Weber APM (2008) Functional characterization of the plastidic phosphate translocator gene family from the thermo-acidophilic red alga Galdieria sulphuraria reveals specific adaptations of primary carbon partitioning in green plants and red algae. Plant Physiol 148: 1487-1496. (Pubitemid 352847513)
110. Mullin KA, Lim L, Ralph SA, Spurck TP, Handman E, McFadden GI (2006) Membrane transporters in the relict plastid of malaria parasites. Proc Natl Acad Sci U S A 103: 9572-9577. (Pubitemid 43955866)
111. Fleige T, Fisher K, Ferguson DJP, Gross U, Bohne W (2007) Carbohydrate metabolism in the Toxoplasma gondii apicoplast: Localization of three glycolytic enzymes, the single pyruvate dehydrogenase complex, and a plastid phosphate translocator. Eukaryotic Cell 6: 984-996. (Pubitemid 46983298)
112. Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, et al. (2012) RobiNA: a user-friendly, integrated software solution for RNA-seq based transcriptomics. Nucleic Acids Res 40: W622-W627,
113. Petersen TN, Brunak S, von Heijne G, Neilsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
114. Marchler-Bauer A, Zheng C, Chitaz F, Derbyshire MK, Geer LY et al. (2013) CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 41: D348-D352.
115. Marck C (1988) 'DNA Strider': a 'C' program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res 16: 1829-1836.
116. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580. (Pubitemid 33032862)
117. Emanuelsson O, Neilsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016.
118. Chou K-C, Shen H-B (2007) Euk-mPLoc: a fusion classifier for large-scale eukaryotic protein subcellular location prediction by incorporating multiple sites. J Proteome Res 6: 1728-1734. (Pubitemid 46814497)
119. Chou K-C, Shen H-B (2010) A new method for predicting the subcellular localization of eukaryotic proteins with both single and multiple sites: Eukm-PLoc 2.0. PLoS ONE 5: e9931.
120. Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Marchler-Bauer (2007) WoLF PSORT: Protein localization predictor. Nucleic Acids Res 35: W585-W587.
121. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066. (Pubitemid 34851225)
122. Maddison DR, Maddison WP (2003) MacClade 4: analysis of phylogeny and character evolution. v. 4.08.
123. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
124. Lartillot N, Lepage T, Blanquart S (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25: 2286-2288.
125. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27: 1164-1165.
126. Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25: 1307-1320. (Pubitemid 351882003)
127. Le SQ, Gascuel O, Lartillot N (2008) Empirical profile mixture models for phylogenetic reconstruction. Bioinformatics 24: 2317-2323.