The Apicoplast

  • Soledad Funes
  • Xochitl Pérez-Martínez
  • Adri án Reyes-Prieto
  • Diego González-Halphen
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 23)

The apicoplast is an essential organelle characteristic of the apicomplexan parasites. It harbors its own genome and it is believed to be a chloroplast-derived organelle that originated by secondary endosymbiosis. Here, we address the more relevant properties of this organelle, an evolutionary relict of a once fully-functional algal chloroplast. We address how its highly-reduced plastid genome replicates and segregates, and how it gets transcribed and translated. We also describe the particular metabolism of the apicoplast, limited to certain pathways, including fatty acid and lipid biosynthesis, the non-mevalonate isoprenoid synthesis pathway, the biosynthesis of iron-sulfur clusters, and the de novo synthesis of heme groups. These metabolic pathways are of relevance as a preferred target for anti-parasitic drugs.


Plastid Genome Transit Peptide Toxoplasma Gondii Apicomplexan Parasite Chloroplast Transit Peptide 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  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 and Kapur V (2004) Com-plete genome sequence of the Apicomplexan, Cryptosporid-ium parvum. Science 304: 441-445PubMedGoogle Scholar
  2. Adam Z and Clarke AK (2002) Cutting edge of chloroplast pro-teolysis. Trends Plant Sci 7: 451-456PubMedGoogle Scholar
  3. Aravind L, Iyer LM, Wellems TE and Miller LH (2003) Plas-modium biology: genomic gleanings. Cell 115: 771-785PubMedGoogle Scholar
  4. Archibald JM and Keeling PJ (2002) Recycled plastids: a “green movement” in eukaryotic evolution. Trends Genet 18: 577-584PubMedGoogle Scholar
  5. Archibald JM and Keeling PJ (2003) Comparative genomics. Plant genomes: cyanobacterial genes revealed. Heredity 90: 2-3PubMedGoogle Scholar
  6. 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 and Whetzel P (2003) PlasmoDB: the Plasmodium genome resource. A database integrating experimental and computa-tional data. Nucleic Acids Res 31: 212-215PubMedGoogle Scholar
  7. Bannister LH, Hopkins JM, Fowler RE, Krishna S and Mitchell GH (2000) A brief illustrated guide to the ultrastructure of Plasmodium falciparum asexual blood stages. Parasitol Today 16: 427-433PubMedGoogle Scholar
  8. Beckers CJ, Roos DS, Donald RG, Luft BJ, Schwab JC, Cao Y and Joiner KA (1995) Inhibition of cytoplasmic and organellar protein synthesis in T. gondii. Implications for the target of macrolide antibiotics. J Clin Invest 95: 367-376PubMedGoogle Scholar
  9. Beeson JG, Winstanley PA, McFadden GI and Brown GV (2001) New agents to combat malaria. Nat Med 7: 149-150PubMedGoogle Scholar
  10. Bendtsen JD, Nielsen H, von Heijne G and Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795PubMedGoogle Scholar
  11. Black MW and Boothroyd JC (2000) Lytic cycle of Toxoplasma gondii. Microbiol Mol Biol Rev 64: 607-623PubMedGoogle Scholar
  12. Blanchard JL and Hicks JS (1999) The non-photosynthetic plas-tid in malarial parasites and other apicomplexans is derived from outside the green plastid lineage. J Eukaryot Microbiol 46: 367-375PubMedGoogle Scholar
  13. Bodyl A (1999) How are plastid proteins of the apicomplexan parasites imported? A hypothesis. Acta Protozool 38: 31-37Google Scholar
  14. Borst P, Overdulve JP, Weijers PJ, Fase-Fowler F and Van den Berg M (1984) DNA circles with cruciforms from Isospora (Toxoplasma) gondii. Biochim Biophys Acta 781: 100-111PubMedGoogle Scholar
  15. Borza T, Popescu CE, and Lee RW (2005) Multiple metabolic roles for the nonphotosynthetic plastid of the green Alga Pro-totheca wickerhamii. Eukaryot Cell 4: 253-261PubMedGoogle Scholar
  16. Bracchi-Ricard V, Nguyen KT, Zhou Y, Rajagopalan PTR, Chakrabarti D and Pei D (2001) Characterization of an eu-karyotic peptide deformylase from Plasmodium falciparum. Arch Biochem Biophys 396: 162-170PubMedGoogle Scholar
  17. Bruce BD (2000) Chloroplast transit peptides: structure, function and evolution. Trends Cell Biol 10: 440-447PubMedGoogle Scholar
  18. Brydges SD and Carruthers VB (2003) Mutation of an unusual mitochondrial targeting sequence of SODB2 produces multi-ple targeting fates in Toxoplasma gondii. J Cell Sci. 116: 4675-4685PubMedGoogle Scholar
  19. Cai X, Fuller AL., McDougald LR and Zhu G (2003) Apicoplast genome of the coccidian Eimeria tenella. Gene 321: 39-46PubMedGoogle Scholar
  20. Campbell EA, Korzheva N, Mustaev A, Murakami K, Nair S, Goldfarb A and Darst SA (2001) Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104: 901-912PubMedGoogle Scholar
  21. Camps M, Arrizabalaga G and Boothroyd, JC (2002) An rRNA mutation identifies the apicoplast as the target for clindamycin in Toxoplasma gondii. Mol Microbiol 43: 1309-1318PubMedGoogle Scholar
  22. Carlton JM, Angiuoli SV, Suh BB, Kooij TW, Pertea M, Silva JC, Ermolaeva MD, Allen JE, Selengut JD, Koo HL, Peterson JD, Pop M, Kosack DS, Shumway MF, Bidwell SL, Shallom SJ, van Aken SE, Riedmuller SB, Feldblyum TV, Cho JK, Quack-enbush J, Sedegah M, Shoaibi A, Cummings LM, Florens L, Yates JR, Raine JD, Sinden RE, Harris MA, Cunningham DA, Preiser PR, Bergman LW, Vaidya AB, van Lin LH, Janse CJ, Waters AP, Smith HO, White OR, Salzberg SL, Venter JC, Fraser CM, Hoffman SL, Gardner MJ and Carucci DJ (2002) Genome sequence and comparative analysis of the model ro-dent malaria parasite Plasmodium yoelli yoelli. Nature 419: 512-519PubMedGoogle Scholar
  23. 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: 347-366PubMedGoogle Scholar
  24. Cavalier-Smith T (2003) Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Philos Trans R Soc Lond B Biol Sci 358: 109-133PubMedGoogle Scholar
  25. Cavalier-Smith T and Beaton MJ (1999) The skeletal function of non-genic nuclear DNA: new evidence from ancient cell chimaeras. Genetica 106: 3-13PubMedGoogle Scholar
  26. Chance M, Warhurst D, Baggaley V and Peters W (1972) Prepara-tion and characterisation of DNA from rodent malarias. Trans R Soc Trop Med Hyg 66: 3-4PubMedGoogle Scholar
  27. Cheresh P, Harrison T, Fujioka H and Haldar K (2002). Targeting the malarial plastid via the parasitophorous vacuole. J Biol Chem 277: 16265-16277PubMedGoogle Scholar
  28. Clough B, Strath M, Preiser P, Denny P and Wilson RJM (1997) Thiostrepton binds to malarial plastid rRNA. FEBS Lett 406: 123-125PubMedGoogle Scholar
  29. Clough B, Rangachari K, Strath M, Preiser PR and Wilson RJM (1999) Antibiotic inhibitors of organellar protein synthesis in Plasmodium falciparum. Protist 150: 189-195PubMedGoogle Scholar
  30. Coombs GH and M üller S (2002) Recent advances in the search for new anti-coccidial drugs. Int J Parasitol 32: 497-508PubMedGoogle Scholar
  31. Creasey A, Mendis K, Carlton J, Williamson D, Wilson I and Carter R (1994) Maternal inheritance of extrachromosomal DNA in malaria parasites. Mol Biochem Parasitol 65: 95-98PubMedGoogle Scholar
  32. Darius AK, Mehlhorn H and Heydorn AO (2004) Effects of toltrazuril and ponazuril on the fine structure and multiplica-tion of tachyzoites of the NC-1 strain of Neospora caninum (a synonym of Hammondia heydorni) in cell cultures. Parasitol Res 92: 453-458PubMedGoogle Scholar
  33. Delwiche CF (1999) Tracing the thread of plastid diversity through the tapestry of life. Am Nat 154: S164-S177PubMedGoogle Scholar
  34. DeRocher A, Hagen CB, Froehlich JE, Feagin JE and Parsons M (2000) Analysis of targeting sequences demonstrates that trafficking to the Toxoplasma gondii plastid branches off the secretory system. J Cell Sci 113: 3969-3977PubMedGoogle Scholar
  35. DeRocher A, Gilbert B, Feagin JE and Parsons M (2005) Dis-section of brefeldin A-sensitive and -insensitive steps in api-coplast protein targeting. J Cell Sci 118: 565-574PubMedGoogle Scholar
  36. Derouin F (2001) Anti-toxoplasmosis drugs. Curr Opin Investig Drugs 2: 1368-1374PubMedGoogle Scholar
  37. Dhanasekaran S, Chandra NR, Chandrasekhar Sagar BK, Rangarajan PN and Padmanaban G (2004) δ;-Aminolevulinic Acid Dehydrates from Plasmodium falciparum: indigenous versus imported. J Biol Chem 279: 6934-6942PubMedGoogle Scholar
  38. Dieckmann-Schuppert AS, Bender S, Holder AA, Haldar K, Schwarz RT (1992) Labeling and initial characterization of polar lipids in cultures of Plasmodium falciparum. Parasitol Res 78: 416-422PubMedGoogle Scholar
  39. Ding M, Clayton C and Soldati D (2000) Toxoplasma gondii catalase: are there peroxisomes in Toxoplasma? J Cell Sci 113: 2409-2419PubMedGoogle Scholar
  40. Diniz JA, Silva EO, Lainson R, and de Souza W (2000) The fine structure of Garnia gonadati and its association with the host cell. Parasitol Res 86: 971-977PubMedGoogle Scholar
  41. Docampo R, de Souza W, Miranda K, Rohloff P and Moreno SN (2005) Acidocalcisomes—conserved from bacteria to man. Nat Rev Microbiol 3: 251-261PubMedGoogle Scholar
  42. Doolittle WF (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14: 307-311PubMedGoogle Scholar
  43. Dore E, Frontali C, Forte T and Fratarcangeli S (1983) Further studies and electron microscopic characterization of Plasmod-ium berghei DNA. Mol Biochem Parasitol 8: 339-352PubMedGoogle Scholar
  44. Dunn PP, Stephens PJ and Shirley MW (1998) Eimeria tenella: two species of extrachromosomal DNA revealed by pulsed-field gel electrophoresis. Parasitol Res 84: 272-275PubMedGoogle Scholar
  45. Dupouy-Camet J (2004) New drugs for the treatment of human parasitic protozoa. Parasitologia. 46: 81-84.Google Scholar
  46. Dzierszinski F, Popescu O, Toursel C, Slomianny C, Yahiaoui B and Tomavo S (1999) The protozoan parasite Toxoplasma gondii expresses two functional plant-like glycolytic enzymes. Implications for evolutionary origin of apicomplexans. J Biol Chem 274: 24888-24895PubMedGoogle Scholar
  47. Egea N and Lang-Unnasch N (1995) Phylogeny of the large extra-chromosomal DNA of organisms in the phylum Apicomplexa. J Eukaryot Microbiol 42: 679-684PubMedGoogle Scholar
  48. Egea N and Lang-Unnasch N (1996) Phylogeny of the large extra-chromosomal DNA of organisms in the phylum Apicomplexa. J Eukaryot Microbiol 43: 158PubMedGoogle Scholar
  49. Elabbadi N, Ancelin ML and Vial HJ (1997) Phospholipid metabolism of serine in Plasmodium-infected erythrocytes in-volves phosphatidylserine and direct serine decarboxylation. Biochem J 324: 435-445PubMedGoogle Scholar
  50. Ellis JT, Morrison DA and Jeffries AC (1998) The phylum Api-complexa: an update on the molecular phylogeny. In: Coombs GH, Vickerman K, Sleigh MA, and Warren A (eds), Evolu-tionary Relationships among Protozoa, pp 255-274. Kluwer, Bostom, USAGoogle Scholar
  51. Ellis KE., Clough B, Saldanha JW and Wilson RJ (2001) Nifs and Sufs in malaria. Mol Microbiol 41: 973-981PubMedGoogle Scholar
  52. Emanuelsson O and von Heijne G (2001) Prediction of organellar targeting signals. Biochim Biophys Acta 1541: 114-119PubMedGoogle Scholar
  53. Escalante AA and Ayala FJ (1995) Evolutionary origin of Plas-modium and other Apicomplexa based on rRNA genes. Proc Natl Acad Sci USA 92: 5793-5797PubMedGoogle Scholar
  54. Fagan TF and Hastings JW (2002) Phylogenetic analysis in-dicates multiple origins of chloroplast glyceraldehyde-3-phosphate dehydrogenase genes in dinoflagellates. Mol Biol Evol 19: 1203-1207PubMedGoogle Scholar
  55. Fast NM, Kissinger JC, Roos DS and Keeling PJ (2001) Nuclear-encoded, plastid-targeted genes suggest a single common ori-gin for apicomplexan and dinoflagellate plastids. Mol Biol Evol 18: 418-426PubMedGoogle Scholar
  56. Feagin JE (1994) The extrachromosomal DNAs of apicomplexan parasites. Annu Rev Microbiol 48: 81-104PubMedGoogle Scholar
  57. Feagin JE (2000) Mitochondrial genome diversity in parasites. Int J Parasitol 30: 371-390PubMedGoogle Scholar
  58. Feagin JE and Drew ME (1995) Plasmodium falciparum: alter-ations in organelle transcript abundance during the erythro-cytic cycle. Exp Parasitol 80: 430-440PubMedGoogle Scholar
  59. Fichera ME and Roos DS (1997) A plastid organelle as a drug target in apicomplexan parasites. Nature 390: 407-409PubMedGoogle Scholar
  60. Fichera ME, Bhopale MK and Roos DS (1995) In vitro assays elucidate peculiar kinetics of clindamycin action against Toxo-plasma gondii. Antimicrob Agents Chemother 39: 1530-1537PubMedGoogle Scholar
  61. Fitzpatrick T, Ricken S, Lanzer M, Amrhein N, Macheroux P and Kappes B (2001) Subcellular localization and characterization of chorismate synthase in the apicomplexan Plasmodium fal-ciparum. Mol Microbiol 40: 65-75PubMedGoogle Scholar
  62. Foth BJ and McFadden GI (2003) The apicoplast: a plastid in Plasmodium falciparum and other Apicomplexan parasites. Int Rev Cytol 224: 57-110PubMedGoogle Scholar
  63. Foth BJ, Ralph SA, Tonkin CJ, Struck NS, Fraunholz M, Roos DS, Cowman AF and McFadden GI (2003) Dissecting api-coplast targeting in the malaria parasite Plasmodium falci-parum. Science 299: 705-708PubMedGoogle Scholar
  64. Foth BJ, Stimmler LM, Handman E, Crabb BS, Hodder AN and McFadden, GI (2005) The malaria parasite Plasmodium falci-parum has only one pyruvate dehydrogenase complex, which is located in the apicoplast. Molecular Microbiology 55: 39-53PubMedGoogle Scholar
  65. Funes S, Davidson E, Reyes-Prieto A, Magallon S, Herion P, King MP and Gonz ález-Halphen D (2002) A green algal apicoplast ancestor. Science 298: 2155PubMedGoogle Scholar
  66. Funes S, Davidson E, Reyes-Prieto A, Magallon S, Herion P, King MP and Gonz ález-Halphen D (2003) Reply to com-ment on “A green algal apicoplast ancestor.” Science 301: 49Google Scholar
  67. Gajadhar AA, Marquardt WC, Hall R, Gunderson J, Ariztia-Carmona E and Sogin ML (1991) Ribosomal RNA sequences of Sarcocystis muris, Theileria annulata and Crypthecodinium cohnii reveal evolutionary relationships among apicomplex-ans, dinoflagellates, and ciliates. Mol Biochem Parasitol 45: 147-154PubMedGoogle Scholar
  68. Gardner MJ, Bates PA, Ling IT, Moore DJ, McCready S, Gunasekera MB, Wilson RJ and Williamson DH (1988) Mi-tochondrial DNA of the human malarial parasite Plasmodium falciparum. Mol Biochem Parasitol 31: 11-18PubMedGoogle Scholar
  69. Gardner MJ, Williamson DH and Wilson RJ (1991a) A circular DNA in malaria parasites encodes an RNA polymerase like that of prokaryotes and chloroplasts. Mol Biochem Parasitol 44: 115-123Google Scholar
  70. Gardner MJ, Feagin JE, Moore DJ, Spencer DF, Gray MW, Williamson DH and Wilson RJ (1991b) Organization and ex-pression of small subunit ribosomal RNA genes encoded by a 35-kilobase circular DNA in Plasmodium falciparum. Mol Biochem Parasitol 48: 77-88Google Scholar
  71. Gardner MJ, Feagin JE, Moore DJ, Rangachari K, Williamson DH and Wilson RJ (1993) Sequence and organization of large subunit rRNA genes from the extrachromosomal 35 kb circular DNA of the malaria parasite Plasmodium falciparum. Nucleic Acids Res 21: 1067-1071PubMedGoogle Scholar
  72. Gardner MJ, Goldman N, Barnett P, Moore PW, Rangachari K, Strath M, Whyte A, Williamson DH and Wilson RJ (1994) Phylogenetic analysis of the rpoB gene from the plastid-like DNA of Plasmodium falciparum. Mol Biochem Parasitol 66: 221-231PubMedGoogle Scholar
  73. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, New-bold C, Davis RW, Fraser CM and Barrell B (2002) Genome sequence of the human malaria parasite Plasmodium falci-parum. Nature 419: 498-511PubMedGoogle Scholar
  74. Gerold P and Schwarz RT (2001) Biosynthesis of glycosphin-golipids de-novo by the human malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 112: 29-37PubMedGoogle Scholar
  75. Gibbs SP (1978) The chloroplasts of Euglena may have evolved from symbiotic green algae. Can J Bot 56: 2882-2889Google Scholar
  76. Gibbs SP (1981) The chloroplasts of some algal groups may have evolved from endosymbiotic eukaryotic algae. Ann NY Acad Sci 361: 193-208PubMedGoogle Scholar
  77. Giglione C, Serero A, Pierre M, Boisson B and Meinnel T (2000) Identification of eukaryotic peptide deformylases re-veals universality of N-terminal protein processing mechanisms. EMBO J 19: 5916-5929PubMedGoogle Scholar
  78. Gleeson MT (2000) The plastid in Apicomplexa: what use is it? Int J Parasitol 30: 1053-1070PubMedGoogle Scholar
  79. Gleeson MT and Johnson AM (1999) Physical characterization of the plastid DNA in Neospora caninum. Int J Parasitol 29: 1563-1573PubMedGoogle Scholar
  80. Gockel G and Hachtel W (2000) Complete gene map of the plastid genome of the nonphotosynthetic euglenoid flagellate Astasia longa. Protist 151: 347-351PubMedGoogle Scholar
  81. Gozalbes R, Brun-Pascaud M, Garcia-Domenech R, Galvez J, Girard PM, Doucet JP and Derouin F (2000) Anti-toxoplasma activities of 24 quinolones and fluoroquinolones in vitro: prediction of activity by molecular topology and virtual compu-tational techniques. Antimicrob Agents Chemother 44: 2771-2776PubMedGoogle Scholar
  82. Gornicki P (2003) Apicoplast fatty acid biosynthesis as a tar-get for medical intervention in apicomplexan parasites. Int J Parasitol 33: 885-896PubMedGoogle Scholar
  83. Gowda DC, Gupta P, Davidson EA (1997) Glycosylphos-phatidylinositol anchors represent the major carbohydrate modification in proteins of intraerythrocytic stage Plasmodium falciparum. J Biol Chem 272: 6428-6439PubMedGoogle Scholar
  84. Gray MW (1999) Evolution of organellar genomes. Curr Opin Genet Dev 9: 678-687PubMedGoogle Scholar
  85. Gray MW, Burger G and Lang BF (2001) The origin and early evolution of mitochondria. Genome Biol 2: 1018.1-1018.5Google Scholar
  86. Gutteridge W, Trigg P and Williamson D (1971) Properties of DNA from some malarial parasites. Parasitology 62: 209-219PubMedGoogle Scholar
  87. Hackett JD, Yoon HS, Bento Soares M, Bonaldo MF, Casavant TL, Scheetz TE, Nosenko T and Bhattacharya (2004) Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Curr Biol 14: 213-218PubMedGoogle Scholar
  88. Hannaert V, Saavedra E, Duffieux F, Szikora JP, Rigden DJ, Michels PA and Opperdoes FR (2003) Plant-like traits asso-ciated with metabolism of Trypanosoma parasites. Proc Natl Acad Sci USA 100: 1067-1071PubMedGoogle Scholar
  89. Harb OS, Chatterjee B, Fraunholz MJ, Crawford MJ, Nishi M and Roos DS (2004) Multiple functionally redundant signals me-diate targeting to the apicoplast in the apicomplexan parasite Toxoplasma gondii. Eukaryot Cell 3: 663-674PubMedGoogle Scholar
  90. Harper JT and Keeling PJ (2003) Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol Biol Evol 20: 1730-1735PubMedGoogle Scholar
  91. He CY, Shaw MK, Pletcher CH, Striepen B, Tilney LG and Roos DS (2001a) A plastid segregation defect in the protozoan par-asite Toxoplasma gondii. EMBO J 20: 330-339Google Scholar
  92. He CY, Striepen B, Pletcher CH, Murray JM and Roos DS (2001b) Targeting and processing of nuclear-encoded api-coplast proteins in plastid segregation mutants of Toxoplasma gondii. J Biol Chem 276: 28436-28442Google Scholar
  93. Henze K, Badr A, Wettern M, Cerff R and Martin W (1995) A nuclear gene of eubacterial origin in Euglena gracilis re-flects cryptic endosymbioses during protist evolution. Proc Natl Acad Sci USA 92: 9122-9126PubMedGoogle Scholar
  94. Hopkins J, Fowler R, Krishna S, Wilson I, Mitchell G and Bannister L (1999) The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protist 150: 283-295PubMedGoogle Scholar
  95. Howe CJ (1992) Plastid origin of an extrachromosomal DNA molecule from Plasmodium, the causative agent of malaria. J Theor Biol 158: 199-205PubMedGoogle Scholar
  96. Huang J, Mullapudi N, Sicheritz-Ponten T and Kissinger JC (2004) A first glimpse into the pattern and scale of gene transfer in the Apicomplexa. Int J Parasitol 34: 265-274PubMedGoogle Scholar
  97. Huang J, Mullapudi N, Lancto CA, Scott M, Abrahamsen MS, and Kissinger JC (2004) Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biol. 5: R88PubMedGoogle Scholar
  98. Jelenska J, Crawford MJ, Harb OS, Zuther E, Hazelkorn R, Roos DS, Gornicki P (2001) Subcellular localization of acetyl-CoA carboxylase in the apicomplexan parasite Toxoplasma gondii. Proc Natl Acad Sci USA 98: 2723-2728PubMedGoogle Scholar
  99. Jelenska J, Sirikhachornkit A, Haselkorn R and Gornicki P (2002) The carboxyltransferase activity of the apicoplast acetyl-CoA carboxylase of Toxoplasma gondii is the target of aryloxyphenoxypropionate inhibitors. J Biol Chem 277: 23208-23215PubMedGoogle Scholar
  100. Jomaa H, Wiesner J, Sanderbrand S, Altincicek B, Weidemeyer C, Hintz M, Turbachova I, Eberl M, Zeidler J, Lichtenthaler HK, Soldati D and Beck E (1999) Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285: 1573-1576PubMedGoogle Scholar
  101. Kaasch AJ and Joiner KA (2000) Targeting and subcellular local-ization of Toxoplasma gondii catalase. Identification of perox-isomes in an apicomplexan parasite. J Biol Chem 275: 1112-1118PubMedGoogle Scholar
  102. Khan SA (2000) Plasmid rolling-circle replication: recent devel-opments. Mol Microbiol 37: 477-484PubMedGoogle Scholar
  103. Kilejian A (1975) Circular mitochondrial DNA from the avian malarial parasite Plasmodium lophurae. Biochim Biophys Acta 390: 276-284PubMedGoogle Scholar
  104. Kilejian A (1991) Sphaerical bodies. Parasitol Today 7: 309PubMedGoogle Scholar
  105. Kissinger JC, Brunk BP, Crabtree J, Fraunholz MJ, Gajria B, Milgram AJ, Pearson DS, Schug J, Bahl A, Diskin SJ, Ginsburg H, Grant GR, Gupta D, Labo P, Li L, Mailman MD, McWeeney SK, Whetzel P, Stoeckert CJ and Roos DS (2002) The Plasmodium genome database. Nature 419: 490-492PubMedGoogle Scholar
  106. Kissinger JC, Gajria B, Li L, Paulsen IT and Roos DS (2003) ToxoDB: accessing the Toxoplasma gondii genome. Nucleic Acids Res 31: 234-236PubMedGoogle Scholar
  107. Knauf U and 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: 492-497Google Scholar
  108. K öhler S, Delwiche CF, Denny PW, Tilney LG, Webster P, Wilson RJ, Palmer JD and Roos DS (1997) A plastid of probable green algal origin in Apicomplexan parasites. Science 275: 1485-1489Google Scholar
  109. Kolodner RD and Tewari KK (1975) Chloroplast DNA from higher plants replicates by both the Cairns and the rolling circle mechanism. Nature 256: 708-711PubMedGoogle Scholar
  110. Khor V, Yowell C, Dame JB and Rowe TC (2005) Expression and characterization of the ATP-binding domain of a malarial Plasmodium vivax gene homologous to the B-subunit of the bacterial topoisomerase DNA gyrase. Mol Biochem Parasitol 140: 107-117PubMedGoogle Scholar
  111. Kroth P and Strotmann H (1999) Diatom plastids: secondary endocyctobiosis, plastid genome and protein import. Physiol Plant 107: 136-141Google Scholar
  112. Lang-Unnasch N and Aiello DP (1999) Sequence evidence for an altered genetic code in the Neospora caninum plastid. Int J Parasitol 29: 1557-1562PubMedGoogle Scholar
  113. Lang-Unnasch N, Reith ME, Munholland J and Barta JR (1998) Plastids are widespread and ancient in parasites of the phylum Apicomplexa. Int J Parasitol 28: 1743-1754PubMedGoogle Scholar
  114. Law AE, Mullineaux CW, Hirst EM, Saldanha J and Wilson RJ (2000) Bacterial orthologues indicate the malarial plastid gene ycf24 is essential. Protist 151: 317-327PubMedGoogle Scholar
  115. Leander BS, Clopton RE and Keeling PJ (2003) Phylogeny of gregarines (Apicomplexa) as inferred from small-subunit rDNA and beta-tubulin. Int J Syst Evol Microbiol 53: 345-354PubMedGoogle Scholar
  116. Lu M and Draper DE (1995) On the role of rRNA tertiary struc-ture in recognition of ribosomal protein L11 and thiostrepton. Nucleic Acids Res 23: 3426-3433PubMedGoogle Scholar
  117. Ludwig M and Gibbs SP (1985) DNA is present in the nucleo-morph of cryptomonads: further evidence that the chloroplast evolved from a eukaryotic endosymbiont. Protoplasma 127: 9-20Google Scholar
  118. Marchesini N, Luo S, Rodrigues CO, Moreno SN and Docampo R (2000) Acidocalcisomes and a vacuolar H+-pyrophosphatase in malaria parasites. Biochem J 347: 243-253PubMedGoogle Scholar
  119. Mar échal E (1997) Lipid synthesis and metabolism in the plastid envelope. Physiol Plant 100: 65-77Google Scholar
  120. Mar échal E and Cesbron-Delauw MF (2001) The apicoplast: a new member of the plastid family. Trends Plant Sci 6: 200-205Google Scholar
  121. Mar échal E, Azzouz N, de Macedo CS, Block MA, Feagin JE, Schwarz RT and Joyard J (2002) Synthesis of chloroplast galactolipids in apicomplexan parasites. Eukaryot Cell 1: 653-656Google Scholar
  122. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M and Penny D (2002) Evolu-tionary analysis of Arabidopsis, cyanobacterial., and chloro-plast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99: 12246-12251PubMedGoogle Scholar
  123. Matsuzaki M, Kikuchi T, Kita K, Kojima S and Kuroiwa T (2001) Large amounts of apicoplast nucleoid DNA and its segregation in Toxoplasma gondii. Protoplasma 218: 180-191PubMedGoogle Scholar
  124. Maul JE, Lilly JW, Cui L, de Pamphilis CW, Miller W, Harris EH and Stern DB (2002) The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14: 2659-2679PubMedGoogle Scholar
  125. McConkey GA, Rogers MJ and McCutchan TF (1997) Inhibi-tion of Plasmodium falciparum protein synthesis. Targeting the plastid-like organelle with thiostrepton. J Biol Chem 272: 2046-2049PubMedGoogle Scholar
  126. McFadden GI and Roos DS (1999) Apicomplexan plastids as drug targets. Trends Microbiol 7: 328-333PubMedGoogle Scholar
  127. McFadden GI and Waller RF (1997) Plastids in parasites of hu-mans. Bioessays 19: 1033-1040PubMedGoogle Scholar
  128. McFadden GI, Gilson PR, Hofmann CJ, Adcock GJ and Maier UG (1994) Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga. Proc Natl Acad Sci USA 91: 3690-3694PubMedGoogle Scholar
  129. McFadden GI, Reith ME, Munholland J and Lang-Unnasch N (1996) Plastid in human parasites. Nature 381: 482PubMedGoogle Scholar
  130. McIntosh MT, Drozdowicz YM, Laroiya K, Rea PA and Vaidya AB (2001) Two classes of plant-like vacuolar-type H(+)-pyrophosphatases in malaria parasites. Mol Biochem Parasitol 114: 183-195PubMedGoogle Scholar
  131. McLeod R, Muench SP, Rafferty JB, Kyle DE, Mui EJ, Kirisits MJ, Mack DG, Roberts CW, Samuel BU, Lyons RE, Dorris M, Milhous WK, and Rice DW (2001) Triclosan inhibits the growth of Plasmodium falciparum and Toxoplasma gondii by inhibition of apicomplexan Fab I. Int J Parasitol 31: 109-113.PubMedGoogle Scholar
  132. Meinnel T (2000) Peptide deformylase of eukaryotic protists: a target for new antiparasitic agents? Parasitol Today 16: 165-168PubMedGoogle Scholar
  133. Miyagishima SY, Nishida K and Kuroiwa T (2003) An evolu-tionary puzzle: chloroplast and mitochondrial division rings. Trends Plant Sci 8: 432-438PubMedGoogle Scholar
  134. Morden CW and Sherwood AR (2002) Continued evolutionary surprises among dinoflagellates. Proc Nat Acad Sci USA 99: 11558-11560PubMedGoogle Scholar
  135. Moreira D and Lopez-Garcia P (2002) The molecular ecology of microbial eukaryotes unveils a hidden world. Trends Micro-biol 10: 31-38Google Scholar
  136. Moreira D and Philippe H (2001) Sure facts and open questions about the origin and evolution of photosynthetic plastids. Res Microbiol 152: 771-780PubMedGoogle Scholar
  137. Neuhaus HE and Emes MJ (2000) Non-photosynthetic metabolism in plastids. Annu Rev Plant Physiol Plant Mol Biol 51: 111-140PubMedGoogle Scholar
  138. Neupert W and Brunner M (2002) The protein import motor of mitochondria. Nat Rev Mol Cell Biol 3: 555-565PubMedGoogle Scholar
  139. Nielsen H, Engelbrecht J, Brunak S and von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering, 10: 1-6PubMedGoogle Scholar
  140. Novick RP (1998) Contrasting lifestyles of rolling-circle phages and plasmids. Trends Biochem Sci 23: 434-438PubMedGoogle Scholar
  141. Obornik M, Jirku M, Slapeta JR, Modry D, Koudela B and Lukes J (2002a) Notes on coccidian phylogeny, based on the api-coplast small subunit ribosomal DNA. Parasitol Res 88: 360-363Google Scholar
  142. Obornik M, Van de Peer Y, Hypsa V, Frickey T, Slapeta JR, Meyer A and Lukes J (2002b) Phylogenetic analyses suggest lateral gene transfer from the mitochondrion to the apicoplast. Gene 285: 109-118Google Scholar
  143. Ohta N, Sato N, Nozaki H and Kuroiwa T (1997) Analysis of the cluster of ribosomal protein genes in the plastid genome of a unicellular red alga Cyanidioschyzon merolae: translocation of the str cluster as an early event in the rhodophyte-chromophyte lineage of plastid evolution. J Mol Evol 45: 688-695PubMedGoogle Scholar
  144. Palmer JD (2003) The symbiotic birth and spread of plastids: how many times and whodunit? J Phycol 39: 1-9Google Scholar
  145. Pandini V, Caprini G, Thomsen N, Aliverti A, Seeber F and Zanetti G (2002) Ferredoxin-NADP+ reductase and ferredoxin of the protozoan parasite Toxoplasma gondii interact produc-tively in vitro and in vivo. J Biol Chem 277: 48463-48471PubMedGoogle Scholar
  146. Patterson D (1999) The diversity of eukaryotes. Am Nat 154: 96-124Google Scholar
  147. P érez-Martínez X, Antaramian A, Vazquez-Acevedo M, Funes S, Tolkunova E, d’Alayer J, Claros MG, Davidson E, King MP and Gonz ález-Halphen D (2001) Subunit II of cytochrome c oxidase in Chlamydomonad algae is a heterodimer encoded by two independent nuclear genes. J Biol Chem 276: 11302-11309Google Scholar
  148. Perozzo R, Kuo M, Sidhu AS, Valiyaveettil JT, Bittman R, Jacobs WR Jr, Fidock DA and Sacchettini JC (2002) Structural elu-cidation of the specificity of the antibacterial agent triclosan for malarial enoyl acyl carrier protein reductase. J Biol Chem 277: 13106-13114PubMedGoogle Scholar
  149. Preiser P, Williamson DH and Wilson RJ (1995) tRNA genes transcribed from the plastid-like DNA of Plasmodium falci-parum. Nucleic Acids Res 23: 4329-4336PubMedGoogle Scholar
  150. Preiser PR, Wilson RJ, Moore PW, McCready S, Hajibagheri MA, Blight KJ, Strath M and Williamson DH (1996) Recom-bination associated with replication of malarial mitochondrial DNA. Embo J 15: 684-693PubMedGoogle Scholar
  151. Puiu D, Enomoto S, Buck GA, Abrahamsen MS and Kissinger JC (2004) CryptoDB: the Cryptosporidium genome resource. Nucleic Acids Res 32: D329-D331PubMedGoogle Scholar
  152. Ralph SA. (2005) Strange organelles-Plasmodium mitochondria lack a pyruvate dehydrogenase complex. Mol Microbiol. 55: 1-4PubMedGoogle Scholar
  153. Ralph SA, D’Ombrain MC and McFadden GI (2001) The api-coplast as an antimalarial drug target. Drug Resist Updat 4: 145-151PubMedGoogle Scholar
  154. Ralph SA, van Dooren GG, Waller RF, Crawford MJ, Fraunholz MJ, Foth BJ, Tonkin CJ, Roos DS, and McFadden GI (2004a) Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2: 203-216.Google Scholar
  155. Ralph SA, Foth BJ, Hall N and McFadden GI (2004b) Evolution-ary pressures on apicoplast transit peptides. Mol Biol Evol. 21: 2183-2194Google Scholar
  156. Ridley RG (1999) Planting the seeds of new antimalarial drugs. Science 285: 1502-1503PubMedGoogle Scholar
  157. Roberts F, Roberts CW, Johnson JJ, Kyle DE, Krell T, Coggins JR, Coombs GH, Milhous WK, Tzipori S, Ferguson DJ, Chakrabarti D and McLeod R (1998) Evidence for the shiki-mate pathway in apicomplexan parasites. Nature 393: 801-805PubMedGoogle Scholar
  158. Roberts CW, Roberts F, Lyons RE, Kirisits MJ, Mui EJ, Finnerty J, Johnson JJ, Ferguson DJ, Coggins JR, Krell T, Coombs GH, Milhous WK, Kyle DE, Tzipori S, Barnwell J, Dame JB, Carlton J and McLeod R (2002) The shikimate path-way and its branches in apicomplexan parasites. J Infect Dis 185: S25-S36PubMedGoogle Scholar
  159. Robibaro B, Hoppe HC, Yang M, Coppens I, Ngo HM, Stedman TT, Paprotka K and Joiner KA (2001) Endocytosis in different lifestyles of protozoan parasitism: role in nutrient uptake with special reference to Toxoplasma gondii. Int J Parasitol 31: 1343-1353PubMedGoogle Scholar
  160. Rogers MJ, Cundliffe E and McCutchan TF (1998) The antibiotic micrococcin is a potent inhibitor of growth and protein syn-thesis in the malaria parasite. Antimicrob Agents Chemother 42: 715-716PubMedGoogle Scholar
  161. Roos DS (1999) The apicoplast as a potential therapeutic tar-get in Toxoplasma and other apicomplexan parasites: some additional thoughts. Parasitol Today 15: 41PubMedGoogle Scholar
  162. Roos DS, Crawford MJ, Donald RG, Kissinger JC, Klimczak LJ and Striepen B (1999) Origin, targeting, and function of the apicomplexan plastid. Curr Opin Microbiol 2: 426-432PubMedGoogle Scholar
  163. Roos DS, Crawford MJ, Donald RG, Fraunholz M, Harb OS, He CY, Kissinger JC, Shaw MK and Striepen B (2002) Mining the Plasmodium genome database to define organellar function: what does the apicoplast do? Philos Trans R Soc Lond B Biol Sci 357: 35-46.PubMedGoogle Scholar
  164. Roy A, Cox RA, Williamson DH and Wilson RJ (1999) Protein synthesis in the plastid of Plasmodium falciparum. Protist 150: 183-188PubMedGoogle Scholar
  165. Ruiz FA, Marchesini N, Seufferheld M, Govindjee and Docampo R (2001) The polyphosphate bodies of Chlamy-domonas reinhardtii possess a proton-pumping pyrophos-phatase and are similar to acidocalcisomes. J Biol Chem 276: 46196-46203PubMedGoogle Scholar
  166. Ryall K, Harper JT and Keeling PJ (2003) Plastid-derived Type II fatty acid biosynthetic enzymes in chromists. Gene 313: 139-148PubMedGoogle Scholar
  167. Ryan PC, Lu M and Draper DE (1991) Recognition of the highly conserved GTPase center of 23 S ribosomal RNA by ribosomal protein L11 and the antibiotic thiostrepton. J Mol Biol 221: 1257-1268PubMedGoogle Scholar
  168. Saldarriaga JF, Taylor FJ, Keeling PJ and Cavalier-Smith T (2001) Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J Mol Evol 53: 204-213PubMedGoogle Scholar
  169. Sato S, Tews I and Wilson RJM (2000) Impact of a plastid-bearing endocytobiont on apicomplexan genomes. Int J Para-sitol 30: 427-439Google Scholar
  170. Scholtyseck E and Piekarski G (1965) Elektronmikroscopische untersuchungen an merozoiten von Eimerien (Eimeria per-forans und E. steidae) und Toxoplasma gondii zur systematis-che stellung von T. gondii. Z Parasiten 26: 93-115Google Scholar
  171. Seeber F (2002) Biogenesis of iron-sulphur clusters in amito-chondriate and apicomplexan protists. Int J Parasitol 32: 1207-1217PubMedGoogle Scholar
  172. Seeber F (2003) Biosynthetic pathways of plastid-derived or-ganelles as potential drug targets against parasitic apicom-plexa. Curr Drug Targets Immune Endocr Metabol Disord 3: 99-109PubMedGoogle Scholar
  173. Siddall ME (1992) Hohlzylinders. Parasitol Today 8: 90-91PubMedGoogle Scholar
  174. Siddall ME, Reece KS, Nerad TA and Burreson EM (2001) Molecular determination of the phylogenetic position of a species in the genus Colpodella (Alveolata). Am Mus Novit 3314: 1-10Google Scholar
  175. Singh D, Chaubey S and Habib S (2003) Replication of the Plasmodium falciparum apicoplast DNA initiates within the inverted repeat region. Mol Biochem Parasitol 126: 9-14PubMedGoogle Scholar
  176. Singh D, Kumar A, Ram EVSR and Habib S (2005) Multiple replication origins within the inverted repeat region of the Plasmodium falciparum apicoplast genome are differentially activated. Mol Biochem Parasitol 139: 99-106PubMedGoogle Scholar
  177. Smeijsters LJ, Zijlstra NM, de Vries E, Franssen FF, Janse CJ and Overdulve JP (1994) The effect of (S)-9-(3-hydroxy-2-phosphonylmethoxypropyl) adenine on nuclear and organellar DNA synthesis in erythrocytic schizogony in malaria. Mol Biochem Parasitol 67: 115-124PubMedGoogle Scholar
  178. Soldati D (1999) The apicoplast as a potential therapeutic target in and other apicomplexan parasites. Parasitol Today 15: 5-7PubMedGoogle Scholar
  179. Soll J and Schleiff E (2004) Plant cell biology: protein import into chloroplasts. Nat Rev Mol Cell Biol 5: 198-208PubMedGoogle Scholar
  180. Stoebe B and Kowallik KV (1999) Gene-cluster analysis in chloroplast genomics. Trends Genet 15: 344-347PubMedGoogle Scholar
  181. Strath M, Scott-Finnigan T, Gardner M, Williamson D and Wilson I (1993) Antimalarial activity of rifampicin in vitro and in rodent models. Trans R Soc Trop Med Hyg 87: 211-216PubMedGoogle Scholar
  182. Striepen B, Crawford MJ, Shaw MK, Tilney LG, Seeber F and Roos DS (2000) The plastid of Toxoplasma gondii is divided by association with the centrosomes. J Cell Biol 151: 1423-1434PubMedGoogle Scholar
  183. Sullivan M, Li J, Kumar S, Rogers MJ and McCutchan TF (2000) Effects of interruption of apicoplast function on malaria infec-tion, development, and transmission. Mol Biochem Parasitol 109: 17-23PubMedGoogle Scholar
  184. Surolia N and Padmanaban G (1992) de novo biosynthesis of heme offers a new chemotherapeutic target in the human malarial parasite. Biochem Biophys Res Commun 187: 744-750PubMedGoogle Scholar
  185. Surolia N and Surolia A (2001) Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP re-ductase of Plasmodium falciparum. Nat Med 7: 167-173PubMedGoogle Scholar
  186. Surolia N, Ramachandra Rao SP and Surolia A (2002) Paradigm shifts in malaria parasite biochemistry and anti-malarial chemotherapy. Bioessays 24: 192-196PubMedGoogle Scholar
  187. Surzycki SJ (1969) Genetic functions of the chloroplast of Chlamydomonas reinhardtii: effect of rifampin on chloroplast DNA-dependent RNA polymerase. Proc Natl Acad Sci USA 63: 1327-1334PubMedGoogle Scholar
  188. Thomsen-Zieger N, Schachtner J and Seeber F (2003) Apicom-plexan parasites contain a single lipoic acid synthase located in the plastid. FEBS Lett 547: 80-86PubMedGoogle Scholar
  189. Touze JE, Fourcade L, Pradines B, Hovette P, Paule P and Heno P (2002) Mechanism of action of antimalarials. Value of com-bined atovaquone/proguanil. Med Trop (Mars) 62: 219-224Google Scholar
  190. Vaidya AB and Arasu P (1987) Tandemly arranged gene clusters of malarial parasites that are highly conserved and transcribed. Mol Biochem Parasitol 22: 249-257PubMedGoogle Scholar
  191. Vaidya AB, Akella R and Suplick K (1989) Sequences similar to genes for two mitochondrial proteins and portions of ribo-somal RNA in a tandemly arrayed 6-kilobase-pair DNA of a malarial parasite. Mol Biochem Parasitol 35: 97-108PubMedGoogle Scholar
  192. van Dooren GG, Waller RF, Joiner KA, Roos DS and McFad-den GI (2000) Traffic jams: protein transport in Plasmodium falciparum. Parasitol Today 16: 421-427PubMedGoogle Scholar
  193. van Dooren GG, Schwartzbach SD, Osafune T and McFadden GI (2001) Translocation of proteins across the multiple mem-branes of complex plastids. Biochim Biophys Acta 1541: 34-53PubMedGoogle Scholar
  194. van Dooren GG, Su V, D’Ombrain MC and McFadden GI (2002) Processing of an apicoplast leader sequence in Plasmodium falciparum and the identification of a putative leader cleavage enzyme. J Biol Chem 277: 23612-23619PubMedGoogle Scholar
  195. Varadharajan S, Sagar BK, Rangarajan PN, and Padmanaban G (2004) Localization of ferrochelatase in Plasmodium falci-parum. Biochem J 384: 429-436PubMedGoogle Scholar
  196. Vial HJ (2000) Isoprenoid biosynthesis and drug targeting in the Apicomplexa. Parasitol Today 16: 140-141PubMedGoogle Scholar
  197. Vivier E and Desportes I (1990) Phylum Apicomplexa. In: Mar-gulis L, Corliss JO, Melkonian M and Chapman DJ (eds), Handbook of Protoctista, pp 549-573. Jones and Bartlett, BostonGoogle Scholar
  198. Vollmer M, Thomsen N, Wiek S and Seeber F (2001) Api-complexan parasites possess distinct nuclear-encoded, but apicoplast-localized, plant-type ferredoxin-NADP+ reductase and ferredoxin. J Biol Chem 276: 5483-5490PubMedGoogle Scholar
  199. Waller RF, Keeling PJ, Donald RG, Striepen B, Handman E, Lang-Unnasch N, Cowman AF, Besra GS, Roos DS and Mc-Fadden GI (1998) Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc Natl Acad Sci USA 95: 12352-12357PubMedGoogle Scholar
  200. Waller RF, Reed MB, Cowman AF and McFadden GI (2000) Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. Embo J 19: 1794-1802PubMedGoogle Scholar
  201. Waller RF, Ralph SA, Reed MB, Su V, Douglas JD, Minnikin DE, Cowman AF, Besra GS, and McFadden GI (2003a) A type II pathway for fatty acid biosynthesis presents drug targets in Plasmodium falciparum. Antimicrob Agents Chemother 47: 297-301Google Scholar
  202. Waller RF, Keeling PJ, van Dooren GG and McFadden GI (2003b) Comment on “A green algal apicoplast ancestor.” Science 301: 49Google Scholar
  203. Waegemann K and Soll J (1996) Phosphorylation of the transit sequence of chloroplast precursor proteins. J Biol Chem. 271: 6545-6554PubMedGoogle Scholar
  204. Weissig V, Vetro-Widenhouse TS and Rowe TC (1997) Topoi-somerase II inhibitors induce cleavage of nuclear and 35-kb plastid DNAs in the malarial parasite Plasmodium falciparum. DNA Cell Biol 16: 1483-1492PubMedGoogle Scholar
  205. Williams BA and Keeling PJ (2003) Cryptic organelles in para-sitic protists and fungi. Adv Parasitol 54: 9-68PubMedGoogle Scholar
  206. Williamson DH, Wilson RJ, Bates PA, McCready S, Perler F and Qiang BU (1985) Nuclear and mitochondrial DNA of the primate malarial parasite Plasmodium knowlesi. Mol Biochem Parasitol 14: 199-209PubMedGoogle Scholar
  207. Williamson DH, Gardner MJ, Preiser P, Moore DJ, Rangachari K and Wilson RJ (1994) The evolutionary origin of the 35 kb circular DNA of Plasmodium falciparum: new evidence supports a possible rhodophyte ancestry. Mol Gen Genet 243: 249-252PubMedGoogle Scholar
  208. Williamson DH, Denny PW, Moore PW, Sato S, McCready S and Wilson RJ (2001) The in vivo conformation of the plastid DNA of Toxoplasma gondii: implications for replication. J Mol Biol 306: 159-168PubMedGoogle Scholar
  209. Williamson DH, Preiser PR, Moore PW, McCready S, Strath M and Wilson RJ (2002) The plastid DNA of the malaria parasite Plasmodium falciparum is replicated by two mechanisms. Mol Microbiol 45: 533-542PubMedGoogle Scholar
  210. Wilson RJM (1991) Reply to “Sphaerical bodies” Parasitol Today 7: 309Google Scholar
  211. Wilson RJM (2002) Progress with parasite plastids. J Mol Biol 319: 257-274PubMedGoogle Scholar
  212. Wilson RJM and Williamson DH (1997) Extrachromosomal DNA in the Apicomplexa. Microbiol Mol Biol Rev 61: 1-16PubMedGoogle Scholar
  213. Wilson RJM, Williamson DH and Preiser P (1994) Malaria and other Apicomplexans: the “plant” connection. Infect Agents Dis 3: 29-37PubMedGoogle Scholar
  214. Wilson RJM, Denny PW, Preiser PR, Rangachari K, Roberts K, Roy A, Whyte A, Strath M, Moore DJ, Moore PW and Williamson DH (1996) Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol 261: 155-172PubMedGoogle Scholar
  215. Wilson RJM, Rangachari K, Saldanha JW, Rickman L, Buxton RS and Eccleston JF (2003) Parasite plastids: maintenance and functions. Philos Trans R Soc Lond B Biol Sci 358: 155-162; discussion 162-164PubMedGoogle Scholar
  216. Wolfe KH, Morden CW and Palmer JD (1992) Function and evolution of a minimal plastid genome from a nonphotosyn-thetic parasitic plant. Proc Natl Acad Sci USA 89: 10648-10652PubMedGoogle Scholar
  217. Wolters J (1991) The troublesome parasites- molecular and morphological evidence that Apicomplexa belong to the dinoflagellate-ciliate clade. Biosystems 25: 75-83PubMedGoogle Scholar
  218. Wrenger C and Muller S (2004) The human malaria parasite Plasmodium falciparum has distinct organelle-specific lipoy-lation pathways. Mol Microbiol. 53:103-113PubMedGoogle Scholar
  219. Yung S and Lang-Unnasch N (1999) Targeting of a nuclear encoded protein to the apicoplast of Toxoplasma gondii. J Eukaryot Microbiol 46: 79S-80SPubMedGoogle Scholar
  220. Zagnitko O, Jelenska J, Tevzadze G, Haselkorn R and Gornicki P (2001) An isoleucine/leucine residue in the carboxyltrans-ferase domain of acetyl-CoA carboxylase is critical for inter-action with aryloxyphenoxypropionate and cyclohexanedione inhibitors. Proc Natl Acad Sci USA 98: 6617-6622PubMedGoogle Scholar
  221. Zuegge J, Ralph S, Schmuker M, McFadden GI and Schneider G (2001) Deciphering apicoplast targeting signals-feature ex-traction from nuclear-encoded precursors of Plasmodium fal-ciparum apicoplast proteins. Gene 280: 19-26PubMedGoogle Scholar
  222. Zhang Z, Green BR and Cavalier-Smith T (1999) Single gene cir-cles in dinoflagellate chloroplast genomes. Nature 400: 155-159PubMedGoogle Scholar
  223. Zhang Z, Green BR and Cavalier-Smith T (2000) Phylogeny of ultra-rapidly evolving dinoflagellate chloroplast genes: A possible common origin for sporozoan and dinoflagellate plastids. J Mol Evol 51: 26-40PubMedGoogle Scholar
  224. Zhu G, Marchewka MJ and Keithly JS (2000a) Cryptosporidium parvum appears to lack a plastid genome. Microbiology 146: 315-321Google Scholar
  225. Zhu G, Marchewka MJ, Woods KM, Upton SJ and Keithly JS (2000b) Molecular analysis of a Type I fatty acid synthase in Cryptosporidium parvum. Mol Biochem Parasitol 105: 253-260Google Scholar
  226. Zuther E, Johnson JJ, Haselkorn R, McLeod R and Gor-nicki P (1999) Growth of Toxoplasma gondii is inhibited by aryloxyphenoxypropionate herbicides targeting acetyl-CoA carboxylase. Proc Natl Acad Sci USA. 96: 13387-13392PubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Soledad Funes
    • 1
  • Xochitl Pérez-Martínez
    • 2
  • Adri án Reyes-Prieto
    • 3
  • Diego González-Halphen
    • 4
  1. 1.Institut f ür Physiologische ChemieLudwig-Maximilians-Universit¨ at MünchenGermany
  2. 2.Departamento de Bioquímica, Instituto de Fisiología CelularUniversidad Nacional Autónoma de MéxicoMexico
  3. 3.Departamento de Botánica, Instituto de BiologíaUniversidad Nacional Autónoma de MéxicoMexico
  4. 4.Departamento de Genética Molecular, Instituto de Fisiología CelularUniversidad Nacional Autónoma de MéxicoMexico

Personalised recommendations