• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of mmbrPermissionsJournals.ASM.orgJournalMMBR ArticleJournal InfoAuthorsReviewers
Microbiol Mol Biol Rev. Mar 1997; 61(1): 1–16.
PMCID: PMC232597

Extrachromosomal DNA in the Apicomplexa.

Abstract

Malaria and related apicomplexan parasites have two highly conserved organellar genomes: one is of plastid (pl) origin, and the other is mitochondrial (mt). The organization of both organellar DNA molecules from the human malaria parasite Plasmodium falciparum has been determined, and they have been shown to be tightly packed with genes. The 35-kb circular DNA is the smallest known vestigial plastid genome and is presumed to be functional. All but two of its recognized genes are involved with genetic expression: one of the two encodes a member of the clp family of molecular chaperones, and the other encodes a conserved protein of unknown function found both in algal plastids and in eubacterial genomes. The possible evolutionary source and intracellular location of the plDNA are discussed. The 6-kb tandemly repeated mt genome is the smallest known and codes for only three proteins (cytochrome b and two subunits of cytochrome oxidase) as well as two bizarrely fragmented rRNAs. The organization of the mt genome differs somewhat among genera. The mtDNA sequence provides information not otherwise available about the structure of apicomplexan cytochrome b as well as the unusually fragmented rRNAs. The malarial mtDNA has a phage-like replication mechanism and undergoes extensive recombination like the mtDNA of some other lower eukaryotes.

Full Text

The Full Text of this article is available as a PDF (705K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Aikawa M. Parasitological review. Plasmodium: the fine structure of malarial parasites. Exp Parasitol. 1971 Oct;30(2):284–320. [PubMed]
  • Aldritt SM, Joseph JT, Wirth DF. Sequence identification of cytochrome b in Plasmodium gallinaceum. Mol Cell Biol. 1989 Sep;9(9):3614–3620. [PMC free article] [PubMed]
  • Araujo FG, Slifer T, Remington JS. Rifabutin is active in murine models of toxoplasmosis. Antimicrob Agents Chemother. 1994 Mar;38(3):570–575. [PMC free article] [PubMed]
  • Baldauf SL, Palmer JD. Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature. 1990 Mar 15;344(6263):262–265. [PubMed]
  • Barta JR, Jenkins MC, Danforth HD. Evolutionary relationships of avian Eimeria species among other Apicomplexan protozoa: monophyly of the apicomplexa is supported. Mol Biol Evol. 1991 May;8(3):345–355. [PubMed]
  • Beckers CJ, Roos DS, Donald RG, Luft BJ, Schwab JC, Cao Y, Joiner KA. Inhibition of cytoplasmic and organellar protein synthesis in Toxoplasma gondii. Implications for the target of macrolide antibiotics. J Clin Invest. 1995 Jan;95(1):367–376. [PMC free article] [PubMed]
  • Black FT, Wildfang IL, Borgbjerg K. Activity of fusidic acid against Plasmodium falciparum in vitro. Lancet. 1985 Mar 9;1(8428):578–579. [PubMed]
  • Boer PH, Gray MW. Scrambled ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA. Cell. 1988 Nov 4;55(3):399–411. [PubMed]
  • Bohne W, Gross U, Ferguson DJ, Heesemann J. Cloning and characterization of a bradyzoite-specifically expressed gene (hsp30/bag1) of Toxoplasma gondii, related to genes encoding small heat-shock proteins of plants. Mol Microbiol. 1995 Jun;16(6):1221–1230. [PubMed]
  • Borst P, Overdulve JP, Weijers PJ, Fase-Fowler F, Van den Berg M. DNA circles with cruciforms from Isospora (Toxoplasma) gondii. Biochim Biophys Acta. 1984 Feb 24;781(1-2):100–111. [PubMed]
  • Cavalier-Smith T. Kingdom protozoa and its 18 phyla. Microbiol Rev. 1993 Dec;57(4):953–994. [PMC free article] [PubMed]
  • Cavalier-Smith T, Allsopp MT, Chao EE. Chimeric conundra: are nucleomorphs and chromists monophyletic or polyphyletic? Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11368–11372. [PMC free article] [PubMed]
  • Chance ML, Warhurst DC, Baggaley VC, Peters W. Preparation and characterization of DNA from rodent malarias. Trans R Soc Trop Med Hyg. 1972;66(1):3–4. [PubMed]
  • Chavalitshewinkoon P, de Vries E, Stam JG, Franssen FF, van der Vliet PC, Overdulve JP. Purification and characterization of DNA polymerases from Plasmodium falciparum. Mol Biochem Parasitol. 1993 Oct;61(2):243–253. [PubMed]
  • Colston MJ, Davis EO. The ins and outs of protein splicing elements. Mol Microbiol. 1994 May;12(3):359–363. [PubMed]
  • Colwell EJ, Hickman RL, Intraprasert R, Tirabutana C. Minocycline and tetracycline treatment of acute falciparum malaria in Thailand. Am J Trop Med Hyg. 1972 Mar;21(2):144–149. [PubMed]
  • Creasey A, Mendis K, Carlton J, Williamson D, Wilson I, Carter R. Maternal inheritance of extrachromosomal DNA in malaria parasites. Mol Biochem Parasitol. 1994 May;65(1):95–98. [PubMed]
  • Creasey AM, Ranford-Cartwright LC, Moore DJ, Williamson DH, Wilson RJ, Walliker D, Carter R. Uniparental inheritance of the mitochondrial gene cytochrome b in Plasmodium falciparum. Curr Genet. 1993;23(4):360–364. [PubMed]
  • Crofts A, Hacker B, Barquera B, Yun CH, Gennis R. Structure and function of the bc-complex of Rhodobacter sphaeroides. Biochim Biophys Acta. 1992 Jul 17;1101(2):162–165. [PubMed]
  • Dore E, Frontali C, Forte T, Fratarcangeli S. Further studies and electron microscopic characterization of Plasmodium berghei DNA. Mol Biochem Parasitol. 1983 Aug;8(4):339–352. [PubMed]
  • Egea N, Lang-Unnasch N. Phylogeny of the large extrachromosomal DNA of organisms in the phylum Apicomplexa. J Eukaryot Microbiol. 1995 Nov-Dec;42(6):679–684. [PubMed]
  • Escalante AA, Ayala FJ. Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11373–11377. [PMC free article] [PubMed]
  • Escalante AA, Ayala FJ. Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes. Proc Natl Acad Sci U S A. 1995 Jun 20;92(13):5793–5797. [PMC free article] [PubMed]
  • Evrard JL, Kuntz M, Straus NA, Weil JH. A class-I intron in a cyanelle tRNA gene from Cyanophora paradoxa: phylogenetic relationship between cyanelles and plant chloroplasts. Gene. 1988 Nov 15;71(1):115–122. [PubMed]
  • Feagin JE. The 6-kb element of Plasmodium falciparum encodes mitochondrial cytochrome genes. Mol Biochem Parasitol. 1992 May;52(1):145–148. [PubMed]
  • Feagin JE. The extrachromosomal DNAs of apicomplexan parasites. Annu Rev Microbiol. 1994;48:81–104. [PubMed]
  • Feagin JE, Drew ME. Plasmodium falciparum: alterations in organelle transcript abundance during the erythrocytic cycle. Exp Parasitol. 1995 May;80(3):430–440. [PubMed]
  • Feagin JE, Gardner MJ, Williamson DH, Wilson RJ. The putative mitochondrial genome of Plasmodium falciparum. J Protozool. 1991 May-Jun;38(3):243–245. [PubMed]
  • Feagin JE, Werner E, Gardner MJ, Williamson DH, Wilson RJ. Homologies between the contiguous and fragmented rRNAs of the two Plasmodium falciparum extrachromosomal DNAs are limited to core sequences. Nucleic Acids Res. 1992 Feb 25;20(4):879–887. [PMC free article] [PubMed]
  • Fichera ME, Bhopale MK, Roos DS. In vitro assays elucidate peculiar kinetics of clindamycin action against Toxoplasma gondii. Antimicrob Agents Chemother. 1995 Jul;39(7):1530–1537. [PMC free article] [PubMed]
  • Fry M, Beesley JE. Mitochondria of mammalian Plasmodium spp. Parasitology. 1991 Feb;102(Pt 1):17–26. [PubMed]
  • Fukuhara H, Sor F, Drissi R, Dinouël N, Miyakawa I, Rousset S, Viola AM. Linear mitochondrial DNAs of yeasts: frequency of occurrence and general features. Mol Cell Biol. 1993 Apr;13(4):2309–2314. [PMC free article] [PubMed]
  • Gajadhar AA, Marquardt WC, Hall R, Gunderson J, Ariztia-Carmona EV, Sogin ML. Ribosomal RNA sequences of Sarcocystis muris, Theileria annulata and Crypthecodinium cohnii reveal evolutionary relationships among apicomplexans, dinoflagellates, and ciliates. Mol Biochem Parasitol. 1991 Mar;45(1):147–154. [PubMed]
  • Gardner MJ, Bates PA, Ling IT, Moore DJ, McCready S, Gunasekera MB, Wilson RJ, Williamson DH. Mitochondrial DNA of the human malarial parasite Plasmodium falciparum. Mol Biochem Parasitol. 1988 Oct;31(1):11–17. [PubMed]
  • Gardner MJ, Feagin JE, Moore DJ, Rangachari K, Williamson DH, Wilson RJ. Sequence and organization of large subunit rRNA genes from the extrachromosomal 35 kb circular DNA of the malaria parasite Plasmodium falciparum. Nucleic Acids Res. 1993 Mar 11;21(5):1067–1071. [PMC free article] [PubMed]
  • Gardner MJ, Feagin JE, Moore DJ, Spencer DF, Gray MW, Williamson DH, Wilson RJ. Organisation and expression of small subunit ribosomal RNA genes encoded by a 35-kilobase circular DNA in Plasmodium falciparum. Mol Biochem Parasitol. 1991 Sep;48(1):77–88. [PubMed]
  • Gardner MJ, Goldman N, Barnett P, Moore PW, Rangachari K, Strath M, Whyte A, Williamson DH, Wilson RJ. Phylogenetic analysis of the rpoB gene from the plastid-like DNA of Plasmodium falciparum. Mol Biochem Parasitol. 1994 Aug;66(2):221–231. [PubMed]
  • Gardner MJ, Preiser P, Rangachari K, Moore D, Feagin JE, Williamson DH, Wilson RJ. Nine duplicated tRNA genes on the plastid-like DNA of the malaria parasite Plasmodium falciparum. Gene. 1994 Jul 8;144(2):307–308. [PubMed]
  • Gardner MJ, Williamson DH, Wilson RJ. A circular DNA in malaria parasites encodes an RNA polymerase like that of prokaryotes and chloroplasts. Mol Biochem Parasitol. 1991 Jan;44(1):115–123. [PubMed]
  • Geary TG, Jensen JB. Effects of antibiotics on Plasmodium falciparum in vitro. Am J Trop Med Hyg. 1983 Mar;32(2):221–225. [PubMed]
  • Gibbs SP. The chloroplasts of some algal groups may have evolved from endosymbiotic eukaryotic algae. Ann N Y Acad Sci. 1981;361:193–208. [PubMed]
  • Gozar MM, Bagnara AS. An organelle-like small subunit ribosomal RNA gene from Babesia bovis: nucleotide sequence, secondary structure of the transcript and preliminary phylogenetic analysis. Int J Parasitol. 1995 Aug;25(8):929–938. [PubMed]
  • Gray MW. The endosymbiont hypothesis revisited. Int Rev Cytol. 1992;141:233–357. [PubMed]
  • Gray MW, Boer PH. Organization and expression of algal (Chlamydomonas reinhardtii) mitochondrial DNA. Philos Trans R Soc Lond B Biol Sci. 1988 May 31;319(1193):135–147. [PubMed]
  • Gritzmacher CA, Reese RT. Protein and nucleic acid synthesis during synchronized growth of Plasmodium falciparum. J Bacteriol. 1984 Dec;160(3):1165–1167. [PMC free article] [PubMed]
  • Gutteridge WE, Trigg PI, Williamson DH. Properties of DNA from some malarial parasites. Parasitology. 1971 Apr;62(2):209–219. [PubMed]
  • Hackstein JH, Mackenstedt U, Mehlhorn H, Meijerink JP, Schubert H, Leunissen JA. Parasitic apicomplexans harbor a chlorophyll a-D1 complex, the potential target for therapeutic triazines. Parasitol Res. 1995;81(3):207–216. [PubMed]
  • Hall R, Coggins L, McKellar S, Shiels B, Tait A. Characterisation of an extrachromosomal DNA element from Theileria annulata. Mol Biochem Parasitol. 1990 Jan 15;38(2):253–260. [PubMed]
  • Hallick RB, Hong L, Drager RG, Favreau MR, Monfort A, Orsat B, Spielmann A, Stutz E. Complete sequence of Euglena gracilis chloroplast DNA. Nucleic Acids Res. 1993 Jul 25;21(15):3537–3544. [PMC free article] [PubMed]
  • Han Z, Stachow C. Analysis of Schizosaccharomyces pombe mitochondrial DNA replication by two dimensional gel electrophoresis. Chromosoma. 1994 Jun;103(3):162–170. [PubMed]
  • Harris EH, Boynton JE, Gillham NW. Chloroplast ribosomes and protein synthesis. Microbiol Rev. 1994 Dec;58(4):700–754. [PMC free article] [PubMed]
  • Howe CJ. Plastid origin of an extrachromosomal DNA molecule from Plasmodium, the causative agent of malaria. J Theor Biol. 1992 Sep 21;158(2):199–205. [PubMed]
  • Basu MK, Wilson HJ. Mercury risk from teeth. Nature. 1991 Jan 10;349(6305):109–109. [PubMed]
  • Hudson GS, Holton TA, Whitfield PR, Bottomley W. Spinach chloroplast rpoBC genes encode three subunits of the chloroplast RNA polymerase. J Mol Biol. 1988 Apr 20;200(4):639–654. [PubMed]
  • Inselburg J, Banyal HS. Synthesis of DNA during the asexual cycle of Plasmodium falciparum in culture. Mol Biochem Parasitol. 1984 Jan;10(1):79–87. [PubMed]
  • Iwata S, Ostermeier C, Ludwig B, Michel H. Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature. 1995 Aug 24;376(6542):660–669. [PubMed]
  • Jasmer DP, Reduker DW, Goff WL, Stiller D, McGuire TC. DNA probes distinguish geographical isolates and identify a novel DNA molecule of Babesia bovis. J Parasitol. 1990 Dec;76(6):834–841. [PubMed]
  • Joseph JT, Aldritt SM, Unnasch T, Puijalon O, Wirth DF. Characterization of a conserved extrachromosomal element isolated from the avian malarial parasite Plasmodium gallinaceum. Mol Cell Biol. 1989 Sep;9(9):3621–3629. [PMC free article] [PubMed]
  • Kairo A, Fairlamb AH, Gobright E, Nene V. A 7.1 kb linear DNA molecule of Theileria parva has scrambled rDNA sequences and open reading frames for mitochondrially encoded proteins. EMBO J. 1994 Feb 15;13(4):898–905. [PMC free article] [PubMed]
  • Kilejian A. Circular mitochondrial DNA from the avian malarial parasite Plasmodium lophurae. Biochim Biophys Acta. 1975 May 16;390(3):276–284. [PubMed]
  • Kilejian A. Spherical bodies. Parasitol Today. 1991 Nov;7(11):309–309. [PubMed]
  • Kostrzewa M, Zetsche K. Large ATP synthase operon of the red alga Antithamnion sp. resembles the corresponding operon in cyanobacteria. J Mol Biol. 1992 Oct 5;227(3):961–970. [PubMed]
  • Lapadat MA, Deerfield DW, 2nd, Pedersen LG, Spremulli LL. Generation of potential structures for the G-domain of chloroplast EF-Tu using comparative molecular modeling. Proteins. 1990;8(3):237–250. [PubMed]
  • Levine ND. Progress in taxonomy of the Apicomplexan protozoa. J Protozool. 1988 Nov;35(4):518–520. [PubMed]
  • Lockhart PJ, Howe CJ, Bryant DA, Beanland TJ, Larkum AW. Substitutional bias confounds inference of cyanelle origins from sequence data. J Mol Evol. 1992 Feb;34(2):153–162. [PubMed]
  • Maleszka R, Clark-Walker GD. In vivo conformation of mitochondrial DNA in fungi and zoosporic moulds. Curr Genet. 1992 Oct;22(4):341–344. [PubMed]
  • Maleszka R, Skelly PJ, Clark-Walker GD. Rolling circle replication of DNA in yeast mitochondria. EMBO J. 1991 Dec;10(12):3923–3929. [PMC free article] [PubMed]
  • McFadden GI, Reith ME, Munholland J, Lang-Unnasch N. Plastid in human parasites. Nature. 1996 Jun 6;381(6582):482–482. [PubMed]
  • Megson A, Inman GJ, Hunt PD, Baylis HA, Hall R. The gene for apocytochrome B of Theileria annulata resides on a small linear extrachromosomal element. Mol Biochem Parasitol. 1991 Sep;48(1):113–115. [PubMed]
  • Nobrega FG, Tzagoloff A. Assembly of the mitochondrial membrane system. DNA sequence and organization of the cytochrome b gene in Saccharomyces cerevisiae D273-10B. J Biol Chem. 1980 Oct 25;255(20):9828–9837. [PubMed]
  • Noller HF. Structure of ribosomal RNA. Annu Rev Biochem. 1984;53:119–162. [PubMed]
  • Ohyama K, Fukuzawa H, Kohchi T, Sano T, Sano S, Shirai H, Umesono K, Shiki Y, Takeuchi M, Chang Z, et al. Structure and organization of Marchantia polymorpha chloroplast genome. I. Cloning and gene identification. J Mol Biol. 1988 Sep 20;203(2):281–298. [PubMed]
  • Olliaro P, Gorini G, Jabes D, Regazzetti A, Rossi R, Marchetti A, Tinelli C, Della Bruna C. In-vitro and in-vivo activity of rifabutin against Toxoplasma gondii. J Antimicrob Chemother. 1994 Nov;34(5):649–657. [PubMed]
  • Ossorio PN, Sibley LD, Boothroyd JC. Mitochondrial-like DNA sequences flanked by direct and inverted repeats in the nuclear genome of Toxoplasma gondii. J Mol Biol. 1991 Dec 5;222(3):525–536. [PubMed]
  • Palmer JD. Rubisco rules fall; gene transfer triumphs. Bioessays. 1995 Dec;17(12):1005–1008. [PubMed]
  • Palmer JD, Delwiche CF. Second-hand chloroplasts and the case of the disappearing nucleus. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7432–7435. [PMC free article] [PubMed]
  • Parsell DA, Kowal AS, Singer MA, Lindquist S. Protein disaggregation mediated by heat-shock protein Hsp104. Nature. 1994 Dec 1;372(6505):475–478. [PubMed]
  • Pfefferkorn ER, Borotz SE. Comparison of mutants of Toxoplasma gondii selected for resistance to azithromycin, spiramycin, or clindamycin. Antimicrob Agents Chemother. 1994 Jan;38(1):31–37. [PMC free article] [PubMed]
  • Pietrokovski S. Conserved sequence features of inteins (protein introns) and their use in identifying new inteins and related proteins. Protein Sci. 1994 Dec;3(12):2340–2350. [PMC free article] [PubMed]
  • Prapunwattana P, O'Sullivan WJ, Yuthavong Y. Depression of Plasmodium falciparum dihydroorotate dehydrogenase activity in in vitro culture by tetracycline. Mol Biochem Parasitol. 1988 Jan 15;27(2-3):119–124. [PubMed]
  • Preiser P, Williamson DH, Wilson RJ. tRNA genes transcribed from the plastid-like DNA of Plasmodium falciparum. Nucleic Acids Res. 1995 Nov 11;23(21):4329–4336. [PMC free article] [PubMed]
  • Preiser PR, Wilson RJ, Moore PW, McCready S, Hajibagheri MA, Blight KJ, Strath M, Williamson DH. Recombination associated with replication of malarial mitochondrial DNA. EMBO J. 1996 Feb 1;15(3):684–693. [PMC free article] [PubMed]
  • Pukrittayakamee S, Viravan C, Charoenlarp P, Yeamput C, Wilson RJ, White NJ. Antimalarial effects of rifampin in Plasmodium vivax malaria. Antimicrob Agents Chemother. 1994 Mar;38(3):511–514. [PMC free article] [PubMed]
  • Read M, Hicks KE, Sims PF, Hyde JE. Molecular characterisation of the enolase gene from the human malaria parasite Plasmodium falciparum. Evidence for ancestry within a photosynthetic lineage. Eur J Biochem. 1994 Mar 1;220(2):513–520. [PubMed]
  • Robson KJ, Gamble Y, Acharya KR. Molecular modelling of malaria calmodulin suggests that it is not a suitable target for novel antimalarials. Philos Trans R Soc Lond B Biol Sci. 1993 Apr 29;340(1291):39–53. [PubMed]
  • de Rojas MO, Wasserman M. Temporal relationships on macromolecular synthesis during the asexual cell cycle of Plasmodium falciparum. Trans R Soc Trop Med Hyg. 1985;79(6):792–796. [PubMed]
  • Rosendahl G, Douthwaite S. The antibiotics micrococcin and thiostrepton interact directly with 23S rRNA nucleotides 1067A and 1095A. Nucleic Acids Res. 1994 Feb 11;22(3):357–363. [PMC free article] [PubMed]
  • Ryan PC, Lu M, Draper DE. Recognition of the highly conserved GTPase center of 23 S ribosomal RNA by ribosomal protein L11 and the antibiotic thiostrepton. J Mol Biol. 1991 Oct 20;221(4):1257–1268. [PubMed]
  • Schelp C, Böse R, Friedhoff KT. Demonstration of extrachromosomal DNA from Babesia equi merozoites. Parasitol Res. 1992;78(8):707–708. [PubMed]
  • Schnare MN, Gray MW. Sixteen discrete RNA components in the cytoplasmic ribosome of Euglena gracilis. J Mol Biol. 1990 Sep 5;215(1):73–83. [PubMed]
  • Scholtyseck E, Mehlhorn H, Hammond DM. Electron microscope studies of microgametogenesis in Coccidia and related groups. Z Parasitenkd. 1972;38(2):95–131. [PubMed]
  • Sena EP, Revet B, Moustacchi E. In vivo homologous recombination intermediates of yeast mitochondrial DNA analyzed by electron microscopy. Mol Gen Genet. 1986 Mar;202(3):421–428. [PubMed]
  • Siddall ME. Hohlzylinders. Parasitol Today. 1992 Mar;8(3):90–91. [PubMed]
  • Smeijsters LJ, Zijlstra NM, de Vries E, Franssen FF, Janse CJ, Overdulve JP. The effect of (S)-9-(3-hydroxy-2-phosphonylmethoxypropyl) adenine on nuclear and organellar DNA synthesis in erythrocytic schizogony in malaria. Mol Biochem Parasitol. 1994 Sep;67(1):115–124. [PubMed]
  • Strath M, Scott-Finnigan T, Gardner M, Williamson D, Wilson I. Antimalarial activity of rifampicin in vitro and in rodent models. Trans R Soc Trop Med Hyg. 1993 Mar-Apr;87(2):211–216. [PubMed]
  • Suplick K, Morrisey J, Vaidya AB. Complex transcription from the extrachromosomal DNA encoding mitochondrial functions of Plasmodium yoelii. Mol Cell Biol. 1990 Dec;10(12):6381–6388. [PMC free article] [PubMed]
  • Surolia N, Padmanaban G. de novo biosynthesis of heme offers a new chemotherapeutic target in the human malarial parasite. Biochem Biophys Res Commun. 1992 Sep 16;187(2):744–750. [PubMed]
  • Thatcher TH, Gorovsky MA. Phylogenetic analysis of the core histones H2A, H2B, H3, and H4. Nucleic Acids Res. 1994 Jan 25;22(2):174–179. [PMC free article] [PubMed]
  • Thompson J, Cundliffe E, Dahlberg AE. Site-directed mutagenesis of Escherichia coli 23 S ribosomal RNA at position 1067 within the GTP hydrolysis centre. J Mol Biol. 1988 Sep 20;203(2):457–465. [PubMed]
  • Tomavo S, Boothroyd JC. Interconnection between organellar functions, development and drug resistance in the protozoan parasite, Toxoplasma gondii. Int J Parasitol. 1995 Nov;25(11):1293–1299. [PubMed]
  • Vaidya AB, Akella R, Suplick K. Sequences similar to genes for two mitochondrial proteins and portions of ribosomal RNA in tandemly arrayed 6-kilobase-pair DNA of a malarial parasite. Mol Biochem Parasitol. 1989 Jun 15;35(2):97–107. [PubMed]
  • Vaidya AB, Arasu P. Tandemly arranged gene clusters of malarial parasites that are highly conserved and transcribed. Mol Biochem Parasitol. 1987 Jan 15;22(2-3):249–257. [PubMed]
  • Vaidya AB, Lashgari MS, Pologe LG, Morrisey J. Structural features of Plasmodium cytochrome b that may underlie susceptibility to 8-aminoquinolines and hydroxynaphthoquinones. Mol Biochem Parasitol. 1993 Mar;58(1):33–42. [PubMed]
  • Vaidya AB, Morrisey J, Plowe CV, Kaslow DC, Wellems TE. Unidirectional dominance of cytoplasmic inheritance in two genetic crosses of Plasmodium falciparum. Mol Cell Biol. 1993 Dec;13(12):7349–7357. [PMC free article] [PubMed]
  • Van de Peer Y, Rensing SA, Maier UG, De Wachter R. Substitution rate calibration of small subunit ribosomal RNA identifies chlorarachniophyte endosymbionts as remnants of green algae. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7732–7736. [PMC free article] [PubMed]
  • Van de Peer Y, Van der Auwera G, De Wachter R. The evolution of stramenopiles and alveolates as derived by "substitution rate calibration" of small ribosomal subunit RNA. J Mol Evol. 1996 Feb;42(2):201–210. [PubMed]
  • Vogel JL, Parsell DA, Lindquist S. Heat-shock proteins Hsp104 and Hsp70 reactivate mRNA splicing after heat inactivation. Curr Biol. 1995 Mar 1;5(3):306–317. [PubMed]
  • Jackson MJ, McArdle A, Edwards RH, Jones DA. Muscle damage in mdx mice. Nature. 1991 Apr 25;350(6320):664–664. [PubMed]
  • Waters AP, White W, McCutchan TF. The structure of the large subunit rRNA expressed in blood stages of Plasmodium falciparum. Mol Biochem Parasitol. 1995 Jun;72(1-2):227–237. [PubMed]
  • Williamson DH, Fennell DJ. Apparent dispersive replication of yeast mitochondrial DNA as revealed by density labelling experiments. Mol Gen Genet. 1974;131(3):193–207. [PubMed]
  • Williamson DH, Gardner MJ, Preiser P, Moore DJ, Rangachari K, Wilson RJ. The evolutionary origin of the 35 kb circular DNA of Plasmodium falciparum: new evidence supports a possible rhodophyte ancestry. Mol Gen Genet. 1994 Apr;243(2):249–252. [PubMed]
  • Williamson DH, Preiser PR, Wilson RJ. Organelle DNAs: The bit players in malaria parasite DNA replication. Parasitol Today. 1996 Sep;12(9):357–362. [PubMed]
  • Williamson DH, Wilson RJ, Bates PA, McCready S, Perler F, Qiang BU. Nuclear and mitochondrial DNA of the primate malarial parasite Plasmodium knowlesi. Mol Biochem Parasitol. 1985 Feb;14(2):199–209. [PubMed]
  • Wilson RJ, Fry M, Gardner MJ, Feagin JE, Williamson DH. Subcellular fractionation of the two organelle DNAs of malaria parasites. Curr Genet. 1992 Apr;21(4-5):405–408. [PubMed]
  • Wilson RJ, Denny PW, Preiser PR, Rangachari K, Roberts K, Roy A, Whyte A, Strath M, Moore DJ, Moore PW, et al. Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol. 1996 Aug 16;261(2):155–172. [PubMed]
  • Wilson RJ, Williamson DH, Preiser P. Malaria and other Apicomplexans: the "plant" connection. Infect Agents Dis. 1994 Feb;3(1):29–37. [PubMed]
  • Wolfe KH, Morden CW, Palmer JD. Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10648–10652. [PMC free article] [PubMed]

Articles from Microbiology and Molecular Biology Reviews : MMBR are provided here courtesy of American Society for Microbiology (ASM)

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...