Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites

eLife

Volumn 4, Issue JULY 2015, 2015, Pages 1-41

  Woo, Yong H ^a   Ansari, Hifzur ^a   Otto, Thomas D ^b   Linger, Christen M K ^c   Olisko, Martin K ^d   Michálek, Jan ^e,f   Saxena, Alka ^a   Shanmugam, Dhanasekaran ^g   Tayyrov, Annageldi ^a   Veluchamy, Alaguraj ^h   Ali, Shahjahan ^a   Bernal, Axel ⁱ   Del Campo, Javier ^d   Cihlář, Jaromír ^e,f   Flegontov, Pavel ^e,j   Gornik, Sebastian G ^k   Hajdušková, Eva ^e   Horák, Aleš ^e,f   Janouškovec, Jan ^d   Katris, Nicholas J ^k   Mast, Fred D ^l   Miranda Saavedra, Diego ^m,n   Mourier, Tobias ^o   Naeem, Raeece ^a   Nair, Mridul ^a   Panigrahi, Aswini K ^a   Rawlings, Neil D ^p   Padron Regalado, Eriko ^a   Ramaprasad, Abhinay ^a   Samad, Nadira ^k   Tomčala, Aleš ^e,f   Wilkes, Jon ^q   Neafsey, Daniel E ^r   Doerig, Christian ^s   Bowler, Chris ^h   Keeling, Patrick J ^d   Roos, David S ⁱ   Dacks, Joel B ^c   Templeton, Thomas J ^t,u   Waller, Ross F ^k,v   Lukeš, Julius ^e,f,w   Oborník, Miroslav ^e,f,x   Pain, Arnab ^a   more..

^a KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF ALBERTA   (Canada)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e INSTITUTE OF PARASITOLOGY   (Czech Republic)

^f UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^g NATIONAL CHEMICAL LABORATORY   (India)

^h INSERM   (France)

ⁱ UNIVERSITY OF PENNSYLVANIA   (United States)

^j UNIVERSITY OF OSTRAVA   (Czech Republic)

^k UNIVERSITY OF MELBOURNE   (Australia)

^l SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^m UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

ⁿ IE BUSINESS SCHOOL   (Spain)

^o UNIVERSITY OF COPENHAGEN   (Denmark)

^p EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^q UNIVERSITY OF GLASGOW   (United Kingdom)

^r BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^s MONASH UNIVERSITY   (Australia)

^t WEILL CORNELL MEDICAL COLLEGE   (United States)

^u NAGASAKI UNIVERSITY   (Japan)

^v UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^w CANADIAN INSTITUTE FOR ADVANCED RESEARCH   (Canada)

^x INSTITUTE OF MICROBIOLOGY   (Czech Republic)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALGA; APICOMPLEXA; ARTICLE; CHROMERA VELIA; GENE EXPRESSION; GENOME ANALYSIS; HOST PARASITE INTERACTION; MOLECULAR EVOLUTION; NONHUMAN; PARASITE; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN LOCALIZATION; RNA ISOLATION; SEQUENCE ALIGNMENT; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; VITRELLA BRASSICAFORMIS; ALVEOLATA; CHEMISTRY; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENETICS; MOLECULAR GENETICS;

ALGAE; ANIMALIA; APICOMPLEXA; EUKARYOTA;

ALGAL DNA;

ALVEOLATA; DNA, ALGAL; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA;

EID: 84937408158     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06974     Document Type: Article

References (177)

1. Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, Deng M, Liu C, Widmer G, Tzipori S, Buck GA, Xu P, Bankier AT, Dear PH, Konfortov BA, Spriggs HF, Iyer L, Anantharaman V, Aravind L, Kapur V. 2004. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304:441–445. doi: 10.1126/science.1094786.
2. Adl SM, Leander BS, Simpson AG, Archibald JM, Anderson OR, Bass D, Bowser SS, Brugerolle G, Farmer MA, Karpov S, Kolisko M, Lane CE, Lodge DJ, Mann DG, Meisterfeld R, Mendoza L, Moestrup O, Mozley-Standridge SE, Smirnov AV, Spiegel F. 2007. Diversity, nomenclature, and taxonomy of protists. Systematic Biology 56: 684–689. doi: 10.1080/10635150701494127.
3. Allen AE, Dupont CL, Oborník M, Horak A, Nunes-Nesi A, Mccrow JP, Zheng H, Johnson DA, Hu H, Fernie AR, Bowler C. 2011. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473: 203–207. doi: 10.1038/nature10074.
4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215:403–410. doi: 10.1016/S0022-2836(05)80360-2.
5. Anantharaman V, Iyer LM, Balaji S, Aravind L. 2007. Adhesion molecules and other secreted host-interaction determinants in Apicomplexa: insights from comparative genomics. International Review of Cytology 262:1–74. doi: 10.1016/S0074-7696(07)62001-4.
6. Aurrecoechea C, Barreto A, Brestelli J, Brunk BP, Cade S, Doherty R, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, Heiges M, Hu S, Iodice J, Kissinger JC, Kraemer ET, Li W, Pinney DF, Pitts B, Roos DS, Srinivasamoorthy G, Stoeckert CJ Jr, Wang H, Warrenfeltz S. 2013. EuPathDB: the eukaryotic pathogen database. Nucleic Acids Research 41:D684–D691. doi: 10.1093/nar/gks1113.
7. Bahl A, Brunk B, Crabtree J, Fraunholz MJ, Gajria B, Grant GR, Ginsburg H, Gupta D, Kissinger JC, Labo P, Li L, Mailman MD, Milgram AJ, Pearson DS, Roos DS, Schug J, Stoeckert CJ Jr, Whetzel P. 2003. PlasmoDB: the Plasmodium genome resource. A database integrating experimental and computational data. Nucleic Acids Research 31:212–215. doi: 10.1093/nar/gkg081.
8. Balaji S, Babu MM, Iyer LM, Aravind L. 2005. Discovery of the principal specific transcription factors of Apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Research 33:3994–4006. doi: 10.1093/nar/gki709.
9. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S. 2002. Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18:298–305. doi: 10.1093/bioinformatics/18.2.298.
10. Bao Z, Eddy SR. 2002. Automated de novo identification of repeat sequence families in sequenced genomes. Genome Research 12:1269–1276. doi: 10.1101/gr.88502.
11. Baum J, Gilberger TW, Frischknecht F, Meissner M. 2008. Host-cell invasion by malaria parasites: insights from Plasmodium and Toxoplasma. Trends in Parasitology 24:557–563. doi: 10.1016/j.pt.2008.08.006.
12. Baum J, Papenfuss AT, Baum B, Speed TP, Cowman AF. 2006. Regulation of apicomplexan actin-based motility. Nature Reviews. Microbiology 4:621–628. doi: 10.1038/nrmicro1465.
13. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. 2004. Improved prediction of signal peptides: SignalP 3.0. Journal of Molecular Biology 340:783–795. doi: 10.1016/j.jmb.2004.05.028.
14. Benson G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research 27: 573–580. doi: 10.1093/nar/27.2.573.
15. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, Hall KP, Evers DJ, Barnes CL, Bignell HR, Boutell JM, Bryant J, Carter RJ, Keira Cheetham R, Cox AJ, Ellis DJ, Flatbush MR, Gormley NA, Humphray SJ, Irving LJ, Karbelashvili MS, Kirk SM, Li H, Liu X, Maisinger KS, Murray LJ, Obradovic B, Ost T, Parkinson ML, Pratt MR, Rasolonjatovo IM, Reed MT, Rigatti R, Rodighiero C, Ross MT, Sabot A, Sankar SV, Scally A, Schroth GP, Smith ME, Smith VP, Spiridou A, Torrance PE, Tzonev SS, Vermaas EH, Walter K, Wu X, Zhang L, Alam MD, Anastasi C, Aniebo IC, Bailey DM, Bancarz IR, Banerjee S, Barbour SG, Baybayan PA, Benoit VA, Benson KF, Bevis C, Black PJ, Boodhun A, Brennan JS, Bridgham JA, Brown RC, Brown AA, Buermann DH, Bundu AA, Burrows JC, Carter NP, Castillo N, Catenazzi E, Chiara M, Chang S, Neil Cooley R, Crake NR, Dada OO, Diakoumakos KD, Dominguez- Fernandez B, Earnshaw DJ, Egbujor UC, Elmore DW, Etchin SS, Ewan MR, Fedurco M, Fraser LJ, Fuentes Fajardo KV, Scott Furey W, George D, Gietzen KJ, Goddard CP, Golda GS, Granieri PA, Green DE, Gustafson DL, Hansen NF, Harnish K, Haudenschild CD, Heyer NI, Hims MM, Ho JT, Horgan AM, Hoschler K, Hurwitz S, Ivanov DV, Johnson MQ, James T, Huw Jones TA, Kang GD, Kerelska TH, Kersey AD, Khrebtukova I, Kindwall AP, Kingsbury Z, Kokko-Gonzales PI, Kumar A, Laurent MA, Lawley CT, Lee SE, Lee X, Liao AK, Loch JA, Lok M, Luo S, Mammen RM, Martin JW, McCauley PG, McNitt P, Mehta P, Moon KW, Mullens JW, Newington T, Ning Z, Ling Ng B, Novo SM, O’Neill MJ, Osborne MA, Osnowski A, Ostadan O, Paraschos LL, Pickering L, Pike AC, Pike AC, Chris Pinkard D, Pliskin DP, Podhasky J, Quijano VJ, Raczy C, Rae VH, Rawlings SR, Chiva Rodriguez A, Roe PM, Rogers J, Rogert Bacigalupo MC, Romanov N, Romieu A, Roth RK, Rourke NJ, Ruediger ST, Rusman E, Sanches-Kuiper RM, Schenker MR, Seoane JM, Shaw RJ, Shiver MK, Short SW, Sizto NL, Sluis JP, Smith MA, Ernest Sohna Sohna J, Spence EJ, Stevens K, Sutton N, Szajkowski L, Tregidgo CL, Turcatti G, Vandevondele S, Verhovsky Y, Virk SM, Wakelin S, Walcott GC, Wang J, Worsley GJ, Yan J, Yau L, Zuerlein M, Rogers J, Mullikin JC, Hurles ME, McCooke NJ, West JS, Oaks FL, Lundberg PL, Klenerman D, Durbin R, Smith AJ. 2008. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456:53–59. doi: 10.1038/nature07517.
16. Bernal A, Crammer K, Hatzigeorgiou A, Pereira F. 2007. Global discriminative learning for higher-accuracy computational gene prediction. PLOS Computational Biology 3:e54. doi: 10.1371/journal.pcbi.0030054.
17. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. 2011. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27:578–579. doi: 10.1093/bioinformatics/btq683.
18. Boetzer M, Pirovano W. 2012. Toward almost closed genomes with GapFiller. Genome Biology 13:R56. doi: 10.1186/gb-2012-13-6-r56.
19. Bolstad BM, Irizarry RA, Astrand M, Speed TP. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185–193. doi: 10.1093/bioinformatics/19.2.185.
20. Bougdour A, Tardieux I, Hakimi MA. 2014. Toxoplasma exports dense granule proteins beyond the vacuole to the host cell nucleus and rewires the host genome expression. Cellular Microbiology 16:334–343. doi: 10.1111/cmi.12255.
21. Box GE, Stuart Hunter J, Hunter WG. 2005. Statistics for experimenters: design, innovation, and discovery. 2nd ed., Wiley series in probability and statistics. Hoboken: Wiley-Interscience.
22. Bullen HE, Tonkin CJ, O’Donnell RA, Tham WH, Papenfuss AT, Gould S, Cowman AF, Crabb BS, Gilson PR. 2009. A novel family of Apicomplexan glideosome-associated proteins with an inner membrane-anchoring role. The Journal of Biological Chemistry 284:25353–25363. doi: 10.1074/jbc.M109.036772.
23. Campbell TL, de Silva EK, Olszewski KL, Elemento O, Llinas M. 2010. Identification and genome-wide prediction of DNA binding specificities for the ApiAP2 family of regulators from the malaria parasite. PLOS Pathogens 6: e1001165. doi: 10.1371/journal.ppat.1001165.
24. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973. doi: 10.1093/bioinformatics/btp348.
25. Caron F, Meyer E. 1989. Molecular basis of surface antigen variation in paramecia. Annual Review of Microbiology 43:23–42. doi: 10.1146/annurev.mi.43.100189.000323.
26. Chaudhry F, Little K, Talarico L, Quintero-Monzon O, Goode BL. 2010. A central role for the WH2 domain of Srv2/ CAP in recharging actin monomers to drive actin turnover in vitro and in vivo. Cytoskeleton 67:120–133. doi: 10.1002/cm.20429.
27. Chen F, Mackey AJ, Stoeckert CJ Jr, Roos DS. 2006. OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Research 34:D363–D368. doi: 10.1093/nar/gkj123.
28. Claros MG, Vincens P. 1996. Computational method to predict mitochondrially imported proteins and their targeting sequences. European Journal of Biochemistry 241:779–786. doi: 10.1111/j.1432-1033.1996.00779.x.
29. Coppens I, Sinai AP, Joiner KA. 2000. Toxoplasma gondii exploits host low-density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. The Journal of Cell Biology 149:167–180. doi: 10.1083/jcb.149.1.167.
30. Csuros M. 2010. Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood. Bioinformatics 26:1910–1912. doi: 10.1093/bioinformatics/btq315.
31. Cumbo VR, Baird AH, Moore RB, Negri AP, Neilan BA, Salih A, van Oppen MJ, Wang Y, Marquis CP. 2013. Chromera velia is endosymbiotic in larvae of the reef corals Acropora digitifera and A. tenuis. Protist 164: 237–244. doi: 10.1016/j.protis.2012.08.003.
32. Danne JC, Gornik SG, Macrae JI, McConville MJ, Waller RF. 2013. Alveolate mitochondrial metabolic evolution: dinoflagellates force reassessment of the role of parasitism as a driver of change in apicomplexans. Molecular Biology and Evolution 30:123–139. doi: 10.1093/molbev/mss205.
33. Du P, Li T, Wang X. 2011. Recent progress in predicting protein sub-subcellular locations. Expert Review of Proteomics 8:391–404. doi: 10.1586/epr.11.20.
34. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32:1792–1797. doi: 10.1093/nar/gkh340.
35. Edgar RC, Myers EW. 2005. PILER: identification and classification of genomic repeats. Bioinformatics 21(Suppl 1): i152–i158. doi: 10.1093/bioinformatics/bti1003.
36. Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M, Wortman JR, Badger JH, Ren Q, Amedeo P, Jones KM, Tallon LJ, Delcher AL, Salzberg SL, Silva JC, Haas BJ, Majoros WH, Farzad M, Carlton JM, Smith RK Jr, Garg J, Pearlman RE, Karrer KM, Sun L, Manning G, Elde NC, Turkewitz AP, Asai DJ, Wilkes DE, Wang Y, Cai H, Collins K, Stewart BA, Lee SR, Wilamowska K, Weinberg Z, Ruzzo WL, Wloga D, Gaertig J, Frankel J, Tsao CC, Gorovsky MA, Keeling PJ, Waller RF, Patron NJ, Cherry JM, Stover NA, Krieger CJ, del Toro C, Ryder HF, Williamson SC, Barbeau RA, Hamilton EP, Orias E. 2006. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLOS Biology 4:e286. doi: 10.1371/journal.pbio.0040286.
37. Ellinghaus D, Kurtz S, Willhoeft U. 2008. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics 9:18. doi: 10.1186/1471-2105-9-18.
38. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2:953–971. doi: 10.1038/nprot.2007.131.
39. Emanuelsson O, Nielsen H, Brunak S, von Heijne G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology 300:1005–1016. doi: 10.1006/jmbi.2000.3903.
40. Faith JJ, Hayete B, Thaden JT, Mogno I, Wierzbowski J, Cottarel G, Kasif S, Collins JJ, Gardner TS. 2007. Largescale mapping and validation of Escherichia coli transcriptional regulation from a compendium of expression profiles. PLOS Biology 5:e8. doi: 10.1371/journal.pbio.0050008.
41. Fedoroff NV. 2012. Presidential address. Transposable elements, epigenetics, and genome evolution. Science 338:758–767. doi: 10.1126/science.338.6108.758.
42. Fehrenbacher K, Huckaba T, Yang HC, Boldogh I, Pon L. 2003. Actin comet tails, endosomes and endosymbionts. The Journal of Experimental Biology 206:1977–1984. doi: 10.1242/jeb.00240.
43. Ferguson DJ, Sahoo N, Pinches RA, Bumstead JM, Tomley FM, Gubbels MJ. 2008. MORN1 has a conserved role in asexual and sexual development across the Apicomplexa. Eukaryot Cell 7:698–711. doi: 10.1128/EC.00021-08.
44. Field HI, Coulson RMR, Field MC. 2013. An automated graphics tool for comparative genomics: the Coulson plot generator. BMC Bioinformatics 14:141. doi: 10.1186/1471-2105-14-141.
45. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M. 2014. Pfam: the protein families database. Nucleic Acids Research 42: D222–D230. doi: 10.1093/nar/gkt1223.
46. Finn RD, Clements J, Eddy SR. 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Research 39:W29–W37. doi: 10.1093/nar/gkr367.
47. Flegontov P, Michalek J, Janouskovec J, Lai DH, Jirku M, Hajduskova E, Tomcala A, Otto TD, Keeling PJ, Pain A, Oborník M, Lukeš J. 2015. Divergent mitochondrial respiratory chains in phototrophic relatives of apicomplexan parasites. Molecular Biology and Evolution 32:1115–1131. doi: 10.1093/molbev/msv021.
48. Flueck C, Bartfai R, Niederwieser I, Witmer K, Alako BT, Moes S, Bozdech Z, Jenoe P, Stunnenberg HG, Voss TS. 2010. A major role for the Plasmodium falciparum ApiAP2 protein PfSIP2 in chromosome end biology. PLOS Pathogens 6:e1000784. doi: 10.1371/journal.ppat.1000784.
49. Flutre T, Duprat E, Feuillet C, Quesneville H. 2011. Considering transposable element diversification in de novo annotation approaches. PLOS ONE 6:e16526. doi: 10.1371/journal.pone.0016526.
50. Folch J, Lees M, Sloane Stanley GH. 1957. A simple method for the isolation and purification of total lipides from animal tissues. The Journal of Biological Chemistry 226:497–509.
51. Foth BJ, Goedecke MC, Soldati D. 2006. New insights into myosin evolution and classification. Proceedings of the National Academy of Sciences of USA 103:3681–3686. doi: 10.1073/pnas.0506307103.
52. Francia ME, Jordan CN, Patel JD, Sheiner L, Demerly JL, Fellows JD, de Leon JC, Morrissette NS, Dubremetz JF, Striepen B. 2012. Cell division in Apicomplexan parasites is organized by a homolog of the striated rootlet fiber of algal flagella. PLOS Biology 10:e1001444. doi: 10.1371/journal.pbio.1001444.
53. Frenal K, Polonais V, Marq JB, Stratmann R, Limenitakis J, Soldati-Favre D. 2010. Functional dissection of the apicomplexan glideosome molecular architecture. Cell Host & Microbe 8:343–357. doi: 10.1016/j.chom.2010.09.002.
54. Frenal K, Soldati-Favre D. 2009. Role of the parasite and host cytoskeleton in Apicomplexa parasitism. Cell Host & Microbe 5:602–611. doi: 10.1016/j.chom.2009.05.013.
55. Gajria B, Bahl A, Brestelli J, Dommer J, Fischer S, Gao X, Heiges M, Iodice J, Kissinger JC, Mackey AJ, Pinney DF, Roos DS, Stoeckert CJ Jr, Wang H, Brunk BP. 2008. ToxoDB: an integrated Toxoplasma gondii database resource. Nucleic Acids Research 36:D553–D556. doi: 10.1093/nar/gkm981.
56. Gandhi M, Jangi M, Goode BL. 2010. Functional surfaces on the actin-binding protein coronin revealed by systematic mutagenesis. The Journal of Biological Chemistry 285:34899–34908. doi: 10.1074/jbc.M110.171496.
57. Gerstein MB, Rozowsky J, Yan KK, Wang D, Cheng C, Brown JB, Davis CA, Hillier L, Sisu C, Li JJ, Pei B, Harmanci AO, Duff MO, Djebali S, Alexander RP, Alver BH, Auerbach R, Bell K, Bickel PJ, Boeck ME, Boley NP, Booth BW, Cherbas L, Cherbas P, Di C, Dobin A, Drenkow J, Ewing B, Fang G, Fastuca M, Feingold EA, Frankish A, Gao G, Good PJ, Guigo R, Hammonds A, Harrow J, Hoskins RA, Howald C, Hu L, Huang H, Hubbard TJ, Huynh C, Jha S, Kasper D, Kato M, Kaufman TC, Kitchen RR, Ladewig E, Lagarde J, Lai E, Leng J, Lu Z, MacCoss M, May G, McWhirter R, Merrihew G, Miller DM, Mortazavi A, Murad R, Oliver B, Olson S, Park PJ, Pazin MJ, Perrimon N, Pervouchine D, Reinke V, Reymond A, Robinson G, Samsonova A, Saunders GI, Schlesinger F, Sethi A, Slack FJ, Spencer WC, Stoiber MH, Strasbourger P, Tanzer A, Thompson OA, Wan KH, Wang G, Wang H, Watkins KL, Wen J, Wen K, Xue C, Yang L, Yip K, Zaleski C, Zhang Y, Zheng H, Brenner SE, Graveley BR, Celniker SE, Gingeras TR, Waterston R. 2014. Comparative analysis of the transcriptome across distant species. Nature 512:445–448. doi: 10.1038/nature13424.
58. Gordon JL, Sibley LD. 2005. Comparative genome analysis reveals a conserved family of actin-like proteins in apicomplexan parasites. BMC Genomics 6:179. doi: 10.1186/1471-2164-6-179.
59. Gournier H, Goley ED, Niederstrasser H, Trinh T, Welch MD. 2001. Reconstitution of human Arp2/3 complex reveals critical roles of individual subunits in complex structure and activity. Molecular Cell 8:1041–1052. doi: 10.1016/S1097-2765(01)00393-8.
60. Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27:221–224. doi: 10.1093/molbev/msp259.
61. Gschloessl B, Guermeur Y, Cock JM. 2008. HECTAR: a method to predict subcellular targeting in heterokonts. BMC Bioinformatics 9:393. doi: 10.1186/1471-2105-9-393.
62. Hafner MS, Sudman PD, Villablanca FX, Spradling TA, Demastes JW, Nadler SA. 1994. Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265:1087–1090. doi: 10.1126/science.8066445.
63. Hager KM, Striepen B, Tilney LG, Roos DS. 1999. The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. Journal of Cell Science 112:2631–2638.
64. Hintze JL, Nelson RD. 1998. Violin plots: a box plot-density trace synergism. American Statistician 52:181–184. doi: 10.2307/2685478.
65. Hirst J, Barlow LD, Francisco GC, Sahlender DA, Seaman MNJ, Dacks JB, Robinson MS. 2011. The fifth adaptor protein complex. PLOS Biology 9:e1001170. doi: 10.1371/journal.pbio.1001170.
66. Hsiao CH, Luisa Hiller N, Haldar K, Knoll LJ. 2013. A HT/PEXEL motif in Toxoplasma dense granule proteins is a signal for protein cleavage but not export into the host cell. Traffic 14:519–531. doi: 10.1111/tra.12049.
67. Hu G, Cabrera A, Kono M, Mok S, Chaal BK, Haase S, Engelberg K, Cheemadan S, Spielmann T, Preiser PR, Gilberger TW, Bozdech Z. 2010. Transcriptional profiling of growth perturbations of the human malaria parasite Plasmodium falciparum. Nature Biotechnology 28:91–98. doi: 10.1038/nbt.1597.
68. Hu K, Johnson J, Florens L, Fraunholz M, Suravajjala S, DiLullo C, Yates J, Roos DS, Murray JM. 2006. Cytoskeletal components of an invasion machine—the apical complex of Toxoplasma gondii. PLOS Pathogens 2:e13. doi: 10.1371/journal.ppat.0020013.
69. Hunt M, Kikuchi T, Sanders M, Newbold C, Berriman M, Otto TD. 2013. REAPR: a universal tool for genome assembly evaluation. Genome Biology 14:R47. doi: 10.1186/gb-2013-14-5-r47.
70. Janouškovec J, Horák A, Barott KL, Rohwer FL, Keeling PJ. 2012. Global analysis of plastid diversity reveals apicomplexan-related lineages in coral reefs. Current Biology 22:R518–R519. doi: 10.1016/j.cub.2012.04.047.
71. Janouškovec J, Horák A, Barott KL, Rohwer FL, Keeling PJ. 2013. Environmental distribution of coral-associated relatives of apicomplexan parasites. The ISME Journal 7:444–447. doi: 10.1038/ismej.2012.129.
72. Janouškovec J, Horák A, Oborník M, Lukeš J, Keeling PJ. 2010. A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proceedings of the National Academy of Sciences of USA 107: 10949–10954. doi: 10.1073/pnas.1003335107.
73. Janouškovec J, Tikhonenkov DV, Burki F, Howe AT, Kolisko M, Mylnikov AP, Keeling PJ. 2015. Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives. Proceedings of the National Academy of Sciences of USA. doi: 10.1073/pnas.1423790112.
74. Johnson LS, Eddy SR, Portugaly E. 2010. Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics 11:431. doi: 10.1186/1471-2105-11-431.
75. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. 2005. Repbase update, a database of eukaryotic repetitive elements. Cytogenetic and Genome Research 110:462–467. doi: 10.1159/000084979.
76. Jurka J, Klonowski P, Dagman V, Pelton P. 1996. CENSOR–a program for identification and elimination of repetitive elements from DNA sequences. Computers and Chemistry 20:119–121. doi: 10.1016/S0097-8485(96)80013-1.
77. Kafsack BF, Rovira-Graells N, Clark TG, Bancells C, Crowley VM, Campino SG, Williams AE, Drought LG, Kwiatkowski DP, Baker DA, Cortes A, Llinas M. 2014. A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature 507:248–252. doi: 10.1038/nature12920.
78. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. 2014. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Research 42:D199–D205. doi: 10.1093/nar/gkt1076.
79. Kaneko I, Iwanaga S, Kato T, Kobayashi I, Yuda M. 2015. Genome-wide identification of the target genes of AP2-O, a plasmodium AP2-family transcription factor. PLOS Pathogens 11:e1004905. doi: 10.1371/journal.ppat.1004905.
80. Katinka MD, Duprat S, Cornillot E, Metenier G, Thomarat F, Prensier G, Barbe V, Peyretaillade E, Brottier P, Wincker P, Delbac F, El Alaoui H, Peyret P, Saurin W, Gouy M, Weissenbach J, Vivares CP. 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450–453. doi: 10.1038/35106579.
81. Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30:772–780. doi: 10.1093/molbev/mst010.
82. Kawase O, Nishikawa Y, Bannai H, Zhang H, Zhang G, Jin S, Lee EG, Xuan X. 2007. Proteomic analysis of calciumdependent secretion in Toxoplasma gondii. Proteomics 7:3718–3725. doi: 10.1002/pmic.200700362.
83. Keeling PJ. 2004. Reduction and compaction in the genome of the apicomplexan parasite Cryptosporidium parvum. Developmental Cell 6:614–616.
84. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14:R36. doi: 10.1186/gb-2013-14-4-r36.
85. Klinger CM, Klute MJ, Dacks JB. 2013a. Comparative genomic analysis of multi-subunit tethering complexes demonstrates an ancient pan-eukaryotic complement and sculpting in Apicomplexa. PLOS ONE 8:e76278. doi: 10.1371/journal.pone.0076278.
86. Klinger CM, Nisbet RE, Ouologuem DT, Roos DS, Dacks JB. 2013b. Cryptic organelle homology in apicomplexan parasites: insights from evolutionary cell biology. Current Opinion in Microbiology 16:424–431. doi: 10.1016/j.mib.2013.07.015.
87. Kolpakov R, Bana G, Kucherov G. 2003. Mreps: efficient and flexible detection of tandem repeats in DNA. Nucleic Acids Research 31:3672–3678. doi: 10.1093/nar/gkg617.
88. Kono M, Herrmann S, Loughran NB, Cabrera A, Engelberg K, Lehmann C, Sinha D, Prinz B, Ruch U, Heussler V, Spielmann T, Parkinson J, Gilberger TW. 2012. Evolution and architecture of the inner membrane complex in asexual and sexual stages of the malaria parasite. Molecular Biology and Evolution 29:2113–2132. doi: 10.1093/molbev/mss081.
89. Kořený L, Oborník M. 2011. Sequence evidence for the presence of two tetrapyrrole pathways in Euglena gracilis. Genome Biology and Evolution 3:359–364. doi: 10.1093/gbe/evr029.
90. Kořeny´ L, Sobotka R, Janouskovec J, Keeling PJ, Oborník M. 2011. Tetrapyrrole synthesis of photosynthetic chromerids is likely homologous to the unusual pathway of apicomplexan parasites. The Plant Cell 23:3454–3462. doi: 10.1105/tpc.111.089102.
91. Koumandou VL, Dacks JB, Coulson RM, Field MC. 2007. Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evolutionary Biology 7:29. doi: 10.1186/1471-2148-7-29.
92. Kozarewa I, Ning Z, Quail MA, Sanders MJ, Berriman M, Turner DJ. 2009. Amplification-free Illumina sequencinglibrary preparation facilitates improved mapping and assembly of (G+C)-biased genomes. Nature Methods 6: 291–295. doi: 10.1038/nmeth.1311.
93. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology 305:567–580. doi: 10.1006/jmbi.2000.4315.
94. Kucera K, Koblansky AA, Saunders LP, Frederick KB, De La Cruz EM, Ghosh S, Modis Y. 2010. Structure-based analysis of Toxoplasma gondii profilin: a parasite-specific motif is required for recognition by Toll-like receptor 11. Journal of Molecular Biology 403:616–629. doi: 10.1016/j.jmb.2010.09.022.
95. Kursula I, Kursula P, Ganter M, Panjikar S, Matuschewski K, Schuler H. 2008. Structural basis for parasite-specific functions of the divergent profilin of Plasmodium falciparum. Structure 16:1638–1648. doi: 10.1016/j.str.2008.09.008.
96. Lartillot N, Philippe H. 2004. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Molecular Biology and Evolution 21:1095–1109. doi: 10.1093/molbev/msh112.
97. Le SQ, Dang CC, Gascuel O. 2012. Modeling protein evolution with several amino acid replacement matrices depending on site rates. Molecular Biology and Evolution 29:2921–2936. doi: 10.1093/molbev/mss112.
98. Lee I, Hong W. 2004. RAP–a putative RNA-binding domain. Trends in Biochemical Sciences 29:567–570. doi: 10.1016/j.tibs.2004.09.005.
99. Leonardi R, Zhang YM, Rock CO, Jackowski S. 2005. Coenzyme A: back in action. Progress in Lipid Research 44: 125–153. doi: 10.1016/j.plipres.2005.04.001.
100. Leung KF, Dacks JB, Field MC. 2008. Evolution of the multivesicular body ESCRT machinery; retention across the eukaryotic lineage. Traffic 9:1698–1716. doi: 10.1111/j.1600-0854.2008.00797.x.
101. Li H, Child MA, Bogyo M. 2012. Proteases as regulators of pathogenesis: examples from the Apicomplexa. Biochimica et Biophysica Acta 1824:177–185. doi: 10.1016/j.bbapap.2011.06.002.
102. Li L, Stoeckert CJ Jr, Roos DS. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Research 13:2178–2189. doi: 10.1101/gr.1224503.
103. Lim L, McFadden GI. 2010. The evolution, metabolism and functions of the apicoplast. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365:749–763. doi: 10.1098/rstb.2009.0273.
104. Liu J, Guo W. 2012. The exocyst complex in exocytosis and cell migration. Protoplasma 249:587–597. doi: 10.1007/s00709-011-0330-1.
105. Logan-Klumpler FJ, de Silva N, Boehme U, Rogers MB, Velarde G, McQuillan JA, Carver T, Aslett M, Olsen C, Subramanian S, Phan I, Farris C, Mitra S, Ramasamy G, Wang H, Tivey A, Jackson A, Houston R, Parkhill J, Holden M, Harb OS, Brunk BP, Myler PJ, Roos D, Carrington M, Smith DF, Hertz-Fowler C, Berriman M. 2012. GeneDB–an annotation database for pathogens. Nucleic Acids Research 40:D98–D108. doi: 10.1093/nar/gkr1032.
106. Machesky LM, Atkinson SJ, Ampe C, Vandekerckhove J, Pollard TD. 1994. Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose. The Journal of Cell Biology 127:107–115. doi: 10.1083/jcb.127.1.107.
107. Magnani E, Sjolander K, Hake S. 2004. From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. The Plant Cell 16:2265–2277. doi: 10.1105/tpc.104.023135.
108. Mazumdar J, Striepen B. 2007. Make it or take it: fatty acid metabolism of apicomplexan parasites. Eukaryot Cell 6: 1727–1735. doi: 10.1128/EC.00255-07.
109. McFadden GI, Reith ME, Munholland J, Lang-Unnasch N. 1996. Plastid in human parasites. Nature 381:482.doi: 10.1038/381482a0.
110. Meyer PE, Lafitte F, Bontempi G. 2008. Minet: a R/Bioconductor package for inferring large transcriptional networks using mutual information. BMC Bioinformatics 9:461. doi: 10.1186/1471-2105-9-461.
111. Miranda K, Pace DA, Cintron R, Rodrigues JCF, Fang J, Smith A, Rohloff P, Coelho E, de Haas F, de SouzaW, Coppens I, Sibley LD, Moreno SNJ. 2010. Characterization of a novel organelle in Toxoplasma gondii with similar composition and function to the plant vacuole. Molecular Microbiology 76:1358–1375. doi: 10.1111/j.1365-2958.2010.07165.x.
112. Moore RB, Oborník M, Janouškovec J, Chrudimsky´ T, Vancová M, Green DH, Wright SW, Davies NW, Bolch CJ, Heimann K, Slapeta J, Hoegh-Guldberg O, Logsdon JM, Carter DA. 2008. A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451:959–963. doi: 10.1038/nature06635.
113. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. 2007. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Research 35:W182–W185. doi: 10.1093/nar/gkm321.
114. Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, Best AA, Cande WZ, Chen F, Cipriano MJ, Davids BJ, Dawson SC, Elmendorf HG, Hehl AB, Holder ME, Huse SM, Kim UU, Lasek-Nesselquist E, Manning G, Nigam A, Nixon JE, Palm D, Passamaneck NE, Prabhu A, Reich CI, Reiner DS, Samuelson J, Svard SG, Sogin ML. 2007. Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317:1921–1926. doi: 10.1126/science.1143837.
115. Morrissette NS, Sibley LD. 2002. Cytoskeleton of apicomplexan parasites. Microbiology and Molecular Biology Reviews 66:21–38. doi: 10.1128/MMBR.66.1.21-38.2002.
116. Mullins RD, Stafford WF, Pollard TD. 1997. Structure, subunit topology, and actin-binding activity of the Arp2/3 complex from Acanthamoeba. The Journal of Cell Biology 136:331–343. doi: 10.1083/jcb.136.2.331.
117. Mundwiler-Pachlatko E, Beck HP. 2013. Maurer’s clefts, the enigma of Plasmodium falciparum. Proceedings of the National Academy of Sciences of USA 110:19987–19994. doi: 10.1073/pnas.1309247110.
118. Mutwil M, Klie S, Tohge T, Giorgi FM, Wilkins O, Campbell MM, Fernie AR, Usadel B, Nikoloski Z, Persson S. 2011. PlaNet: combined sequence and expression comparisons across plant networks derived from seven species. The Plant Cell 23:895–910. doi: 10.1105/tpc.111.083667.
119. Nevin WD, Dacks JB. 2009. Repeated secondary loss of adaptin complex genes in the Apicomplexa. Parasitology International 58:86–94. doi: 10.1016/j.parint.2008.12.002.
120. Oborník M, Modry´ D, Lukeš M, Cernotíková-Stříbrná E, Cihlář J, Tesařová M, Kotabová E, Vancová M, Prášil O, Lukeš J. 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. doi: 10.1016/j.protis.2011.09.001.
121. Oborník M, Vancová M, Lai DH, Janouškovec J, Keeling PJ, Lukeš J. 2011. Morphology and ultrastructure of multiple life cycle stages of the photosynthetic relative of Apicomplexa, Chromera velia. Protist 162:115–130. doi: 10.1016/j.protis.2010.02.004.
122. Okamoto N, Keeling PJ. 2014. The 3D structure of the apical complex and association with the flagellar apparatus revealed by serial TEM tomography in Psammosa pacifica, a distant relative of the Apicomplexa. PLOS ONE 9: e84653. doi: 10.1371/journal.pone.0084653.
123. Otto TD, Sanders M, Berriman M, Newbold C. 2010. Iterative Correction of Reference Nucleotides (iCORN) using second generation sequencing technology. Bioinformatics 26:1704–1707. doi: 10.1093/bioinformatics/btq269.
124. Pawlowski J, Audic S, Adl S, Bass D, Belbahri L, Berney C, Bowser SS, Cepicka I, Decelle J, Dunthorn M, Fiore- Donno AM, Gile GH, Holzmann M, Jahn R, Jirku M, Keeling PJ, Kostka M, Kudryavtsev A, Lara E, Lukeš J, Mann DG, Mitchell EA, Nitsche F, Romeralo M, Saunders GW, Simpson AG, Smirnov AV, Spouge JL, Stern RF, Stoeck T, Zimmermann J, Schindel D, de Vargas C. 2012. CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLOS Biology 10:e1001419. doi: 10.1371/journal.pbio.1001419.
125. Pelletier L, Stern C, Pypaert M, Sheff D. 2002. Golgi biogenesis in Toxoplasma gondii. Nature 418:1–5. doi: 10.1038/nature00946.
126. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8:785–786. doi: 10.1038/nmeth.1701.
127. Petsalaki EI, Bagos PG, Litou ZI, Hamodrakas SJ. 2006. PredSL: a tool for the N-terminal sequence-based prediction of protein subcellular localization. Genomics, Proteomics & Bioinformatics 4:48–55. doi: 10.1016/S1672-0229(06)60016-8.
128. Pieperhoff MS, Schmitt M, Ferguson DJ, Meissner M. 2013. The role of clathrin in post-Golgi trafficking in Toxoplasma gondii. PLOS ONE 8:e77620. doi: 10.1371/journal.pone.0077620.
129. Pombert JF, Blouin NA, Lane C, Boucias D, Keeling PJ. 2014. A lack of parasitic reduction in the obligate parasitic green alga Helicosporidium. PLOS Genetics 10:e1004355. doi: 10.1371/journal.pgen.1004355.
130. Pollard TD, Borisy GG. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112: 453–465. doi: 10.1016/S0092-8674(03)00120-X.
131. Portman N, Foster C, Walker G, Slapeta J. 2014. Evidence of intraflagellar transport and apical complex formation in a free-living relative of the Apicomplexa. Eukaryot Cell 13:10–20. doi: 10.1128/EC.00155-13.
132. Poulin B, Patzewitz EM, Brady D, Silvie O, Wright MH, Ferguson DJ, Wall RJ, Whipple S, Guttery DS, Tate EW, Wickstead B, Holder AA, Tewari R. 2013. Unique apicomplexan IMC sub-compartment proteins are early markers for apical polarity in the malaria parasite. Biology Open 2:1160–1170. doi: 10.1242/bio.20136163.
133. Quail MA, Smith M, Coupland P, Otto TD, Harris SR, Connor TR, Bertoni A, Swerdlow HP, Gu Y. 2012. A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genomics 13:341. doi: 10.1186/1471-2164-13-341.
134. Quesneville H, Nouaud D, Anxolabehere D. 2003. Detection of new transposable element families in Drosophila melanogaster and Anopheles gambiae genomes. Journal of Molecular Evolution 57(Suppl 1):S50–S59. doi: 10.1007/s00239-003-0007-2.
135. Quigg A, Kotabova E, Jaresova J, Kana R, Setlik J, Sediva B, Komarek O, Prasil O. 2012. Photosynthesis in Chromera velia represents a simple system with high efficiency. PLOS ONE 7:e47036. doi: 10.1371/journal.pone.0047036.
136. Radke JB, Lucas O, de Silva EK, Ma Y, Sullivan WJ Jr, Weiss LM, Llinas M, White MW. 2013. ApiAP2 transcription factor restricts development of the Toxoplasma tissue cyst. Proceedings of the National Academy of Sciences of USA 110:6871–6876. doi: 10.1073/pnas.1300059110.
137. Raffaele S, Kamoun S. 2012. Genome evolution in filamentous plant pathogens: why bigger can be better. Nature Reviews. Microbiology 10:417–430. doi: 10.1038/nrmicro2790.
138. Ravindran S, Boothroyd JC. 2008. Secretion of proteins into host cells by Apicomplexan parasites. Traffic 9: 647–656. doi: 10.1111/j.1600-0854.2008.00723.x.
139. Reid AJ, Blake DP, Ansari HR, Billington K, Browne HP, Bryant J, Dunn M, Hung SS, Kawahara F, Miranda-Saavedra D, Malas TB, Mourier T, Naghra H, Nair M, Otto TD, Rawlings ND, Rivailler P, Sanchez-Flores A, Sanders M, Subramaniam C, Tay YL, Woo Y, Wu X, Barrell B, Dear PH, Doerig C, Gruber A, Ivens AC, Parkinson J, Rajandream MA, Shirley MW, Wan KL, Berriman M, Tomley FM, Pain A. 2014. Genomic analysis of the causative agents of coccidiosis in domestic chickens. Genome Research 24:1676–1685. doi: 10.1101/gr.168955.113.
140. Roiko MS, Carruthers VB. 2009. New roles for perforins and proteases in apicomplexan egress. Cellular Microbiology 11:1444–1452. doi: 10.1111/j.1462-5822.2009.01357.x.
141. Roos DS. 2005. Genetics. Themes and variations in apicomplexan parasite biology. Science 309:72–73. doi: 10.1126/science.1115252.
142. Russell K, Hasenkamp S, Emes R, Horrocks P. 2013. Analysis of the spatial and temporal arrangement of transcripts over intergenic regions in the human malarial parasite Plasmodium falciparum. BMC Genomics 14:267. doi: 10.1186/1471-2164-14-267.
143. Rybakin V, Clemen CS. 2005. Coronin proteins as multifunctional regulators of the cytoskeleton and membrane trafficking. Bioessays 27:625–632. doi: 10.1002/bies.20235.
144. Sakharkar KR, Dhar PK, Chow VT. 2004. Genome reduction in prokaryotic obligatory intracellular parasites of humans: a comparative analysis. International Journal of Systematic and Evolutionary Microbiology 54: 1937–1941. doi: 10.1099/ijs.0.63090-0.
145. Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S, Koyanagi R, Takeuchi T, Hisata K, Tanaka M, Fujiwara M, Hamada M, Seidi A, Fujie M, Usami T, Goto H, Yamasaki S, Arakaki N, Suzuki Y, Sugano S, Toyoda A, Kuroki Y, Fujiyama A, Medina M, Coffroth MA, Bhattacharya D, Satoh N. 2013. Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Current Biology 23:1399–1408. doi: 10.1016/j.cub.2013.05.062.
146. Silflow CD, Lefebvre PA. 2001. Assembly and motility of eukaryotic cilia and flagella. Lessons from Chlamydomonas reinhardtii. Plant Physiology 127:1500–1507. doi: 10.1104/pp.010807.
147. Simpson JT, Durbin R. 2012. Efficient de novo assembly of large genomes using compressed data structures. Genome Research 22:549–556. doi: 10.1101/gr.126953.111.
148. Singh BK, Sattler JM, Chatterjee M, Huttu J, Schuler H, Kursula I. 2011. Crystal structures explain functional differences in the two actin depolymerization factors of the malaria parasite. The Journal of Biological Chemistry 286:28256–28264. doi: 10.1074/jbc.M111.211730.
149. Sinha A, Hughes KR, Modrzynska KK, Otto TD, Pfander C, Dickens NJ, Religa AA, Bushell E, Graham AL, Cameron R, Kafsack BF, Williams AE, Llinas M, Berriman M, Billker O, Waters AP. 2014. A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium. Nature 507:253–257. doi: 10.1038/nature12970.
150. Skillman KM, Diraviyam K, Khan A, Tang K, Sept D, Sibley LD. 2011. Evolutionarily divergent, unstable filamentous actin is essential for gliding motility in apicomplexan parasites. PLOS Pathogens 7:e1002280. doi: 10.1371/journal.ppat.1002280.
151. Soldati-Favre D. 2008. Molecular dissection of host cell invasion by the apicomplexans: the glideosome. Parasite 15:197–205.
152. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. doi: 10.1093/bioinformatics/btu033.
153. Stanke M, Keller O, Gunduz I, Hayes A, Waack S, Morgenstern B. 2006. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Research 34:W435–W439. doi: 10.1093/nar/gkl200.
154. Stevens JM, Galyov EE, Stevens MP. 2006. Actin-dependent movement of bacterial pathogens. Nature Reviews. Microbiology 4:91–101. doi: 10.1038/nrmicro1320.
155. Struck NS, Herrmann S, Schmuck-Barkmann I, de Souza Dias S, Haase S, Cabrera AL, Treeck M, Bruns C, Langer C, Cowman AF, Marti M, Spielmann T, Gilberger TW. 2008. Spatial dissection of the cis- and trans-Golgi compartments in the malaria parasite Plasmodium falciparum. Molecular Microbiology 67:1320–1330. doi: 10.1111/j.1365-2958.2008.06125.x.
156. Stuart JM, Segal E, Koller D, Kim SK. 2003. A gene-coexpression network for global discovery of conserved genetic modules. Science 302:249–255. doi: 10.1126/science.1087447.
157. Sutak R, Slapeta J, San Roman M, Camadro JM, Lesuisse E. 2010. Nonreductive iron uptake mechanism in the marine alveolate Chromera velia. Plant Physiology 154:991–1000. doi: 10.1104/pp.110.159947.
158. Tempel S. 2012. Using and understanding RepeatMasker. Methods in Molecular Biology 859:29–51. doi: 10.1007/978-1-61779-603-6_2.
159. Templeton TJ, Iyer LM, Anantharaman V, Enomoto S, Abrahante JE, Subramanian GM, Hoffman SL, Abrahamsen MS, Aravind L. 2004a. Comparative analysis of Apicomplexa and genomic diversity in eukaryotes. Genome Research 14:1686–1695. doi: 10.1101/gr.2615304.
160. Templeton TJ, Lancto CA, Vigdorovich V, Liu C, London NR, Hadsall KZ, Abrahamsen MS. 2004b. The Cryptosporidium oocyst wall protein is a member of a multigene family and has a homolog in Toxoplasma. Infection and Immunity 72:980–987. doi: 10.1128/IAI.72.2.980-987.2004.
161. Tenter AM, Heckeroth AR, Weiss LM. 2000. Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30:1217–1258. doi: 10.1016/S0020-7519(00)00124-7.
162. Tomavo S, Slomianny C, Meissner M, Carruthers VB. 2013. Protein trafficking through the endosomal system prepares intracellular parasites for a home invasion. PLOS Pathogens 9:e1003629. doi: 10.1371/journal.ppat.1003629.
163. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols 7:562–578. doi: 10.1038/nprot.2012.016.
164. Treeck M, Sanders JL, Elias JE, Boothroyd JC. 2011. The phosphoproteomes of Plasmodium falciparum and Toxoplasma gondii reveal unusual adaptations within and beyond the parasites’ boundaries. Cell Host & Microbe 10:410–419. doi: 10.1016/j.chom.2011.09.004.
165. Tsai IJ, Otto TD, Berriman M. 2010. Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps. Genome Biology 11:R41. doi: 10.1186/gb-2010-11-4-r41.
166. Van de Peer Y, Frickey T, Taylor J, Meyer A. 2002. Dealing with saturation at the amino acid level: a case study based on anciently duplicated zebrafish genes. Gene 295:205–211. doi: 10.1016/S0378-1119(02)00689-3.
167. van Dooren GG, Kennedy AT, McFadden GI. 2012. The use and abuse of heme in apicomplexan parasites. Antioxidants & Redox Signaling 17:634–656. doi: 10.1089/ars.2012.4539.
168. Wilson D, Charoensawan V, Kummerfeld SK, Teichmann SA. 2008. DBD—taxonomically broad transcription factor predictions: new content and functionality. Nucleic Acids Research 36:D88–D92.
169. Wong W, Webb AI, Olshina MA, Infusini G, Tan YH, Hanssen E, Catimel B, Suarez C, Condron M, Angrisano F, Nebi T, Kovar DR, Baum J. 2014. A mechanism for actin filament severing by malaria parasite actin depolymerizing factor 1 via a low affinity binding interface. The Journal of Biological Chemistry 289:4043–4054. doi: 10.1074/jbc.M113.523365.
170. Woo Y, Affourtit J, Daigle S, Viale A, Johnson K, Naggert J, Churchill G. 2004. A comparison of cDNA, oligonucleotide, and Affymetrix GeneChip gene expression microarray platforms. Journal of Biomolecular Techniques 15:276–284.
171. Woo YH, Li WH. 2011. Gene clustering pattern, promoter architecture, and gene expression stability in eukaryotic genomes. Proceedings of the National Academy of Sciences of USA 108:3306–3311. doi: 10.1073/pnas.1100210108.
172. Wu TD, Nacu S. 2010. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26:873–881. doi: 10.1093/bioinformatics/btq057.
173. Xu P, Widmer G, Wang Y, Ozaki LS, Alves JM, Serrano MG, Puiu D, Manque P, Akiyoshi D, Mackey AJ, Pearson WR, Dear PH, Bankier AT, Peterson DL, Abrahamsen MS, Kapur V, Tzipori S, Buck GA. 2004. The genome of Cryptosporidium hominis. Nature 431:1107–1112. doi: 10.1038/nature02977.
174. Xu Z, Wang H. 2007. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Research 35:W265–W268. doi: 10.1093/nar/gkm286.
175. Zahradnickova H, Tomcala A, Berkova P, Schneedorferova I, Okrouhlik J, Simek P, Hodkova M. 2014. Cost effective, robust, and reliable coupled separation techniques for the identification and quantification of phospholipids in complex biological matrices: application to insects. Journal of Separation Science 37: 2062–2068.
176. Zdobnov EM, Apweiler R. 2001. InterProScan–an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848. doi: 10.1093/bioinformatics/17.9.847.
177. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Research 18:821–829. doi: 10.1101/gr.074492.107.