Plastids in apicomplexan parasites

  • Chapter
Origins of Algae and their Plastids

Part of the book series: Plant Systematics and Evolution ((SYSTEMATICS,volume 11))

Abstract

The discovery in malarial and toxoplasmodial parasites of genes normally occurring in the photosynthetic organelle of plants and algae has prompted speculation that these so-called protozoans might harbour a vestigial plastid. The plastid-like parasite genes occur on an extrachromosomal, maternally inherited, 35 kb DNA circle with an architecture reminiscent of plastid genomes. The 35kb genome is distinct from the 6–7 kb linear mitochondrial genome. Localization of the 35kb genome within the parasite cells by high resolution in situ hybridization has identified a multi membrane-bound organelle in which the plastid-like genome resides. Since phylogenetic trees incorporating genes from the 35 kb genome group them within the plastid radiation, we believe that the parasite organelle is a reduced plastid, that is probably no longer photosynthetic. Combined molecular and ultrastructural evidence indicate plastids to be widespread among apicomplexan parasites. The origin and role of the plastid in obligate intracellular parasites is completely unknown. The potential utility of the plastid as a parasite-specific target for therapeutic agents is examined.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

eBook
EUR 9.99
Price includes VAT (Germany)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  • Aikawa, M., 1966: The fine structure of the erythrocytic stage of three avian malarial parasites, Plasmodium fallax, P. lophyrae, and P. cathemerium. — Amer. J. Trop. Med. Hyg. 15: 449–471.

    CAS  Google Scholar 

  • Hff, C.G., Strome, C. P. A., 1970: Morphological study of macrogametogenesis of Leucocytozoon simondi. — J. Ultrastruct. Res. 32: 43–68.

    Google Scholar 

  • Aldritt, S. M., Joseph, J. T., Wirth, D. F., 1989: Sequence identification of cytochrome b in Plasmodium gallinaceum. — Molec. Cell. Biol. 9: 3614–3620.

    PubMed  CAS  Google Scholar 

  • Azevedo, C., 1989: Fine structure of Perkinsus atlanticus, new species (Apicomplexa, Perkinsea), Parasite of the clam Ruditapes decussatus from Portugal. — J. Parasitol. 75: 627–635.

    PubMed  CAS  Google Scholar 

  • Baldauf, S. L., Palmer, J. D., 1993: Animals and fungi are each other’s closest relatives: congruent evidence from multiple proteins. — Proc. Natl. Acad. Sci. USA 90: 11558–11562.

    PubMed  CAS  Google Scholar 

  • Bardele, C. F., 1996: Elektronmikroskopische Untersuchungen an dem Sporozoon Eucoccidium dinophili Grell. — Z. Zellforsch. 74: 559–595.

    Google Scholar 

  • Barta, J. R., Jenkins, M. C., Danforth, H. D., 1991: Evolutionary relationships of avian Eimeria spp. among other apicomplexan protozoa: monophyly of the Apicomplexa is supported. — Molec. Biol. Evol. 8: 345–355.

    PubMed  CAS  Google Scholar 

  • Beckers, C. J. M., Roos, D. S., Donald, R. G. K., Luft, B. J., Schwab, J. C., Cao, Y., Joiner, K. A., 1995: Inhibition of cytoplasmic and organellar protein synthesis in Toxoplasma gondii: implications for the target of macrolide antibiotics. — J. Clin. Invest. 95: 367–376.

    PubMed  CAS  Google Scholar 

  • Bhattacharya, D., Helmchen, T., Melkonian, M., 1995: Molecular evolutionary analyses of nuclear-encoded small subunit ribosomal RNA identify an independent rhizopod lineage containing the Euglyphidae and the Chlorarachniophyta. — J. Euk. Microbiol. 42: 65–69.

    PubMed  CAS  Google Scholar 

  • Borst, P., Overdlve, J. P., Weijers, R. J., Fase-Fowler, F., Berg, M. V. D., 1984: DNA circles with cruciforms from Isospora (Toxoplasma) gondii. — Biochim. Biophys. Acta 781: 100–111.

    PubMed  CAS  Google Scholar 

  • Bradley, D. J., Warhurst, D. C., 1995: Malaria prophylaxis: guidelines for travellers from Britian. — Brit. Med. J. 310: 709–714.

    PubMed  CAS  Google Scholar 

  • Brown, P., 1994: Guarded welcome for malaria vaccine. — New Scientist 1994: 14–15.

    Google Scholar 

  • Brugerolle, G., Mignot, J. P., 1979: Observations sur le cycle i’ultrastructure et la position systématique de Spiromonas perforons (Bodo perforons Hollande 1938), flagelle parasite de Chilomonas paramaecium: ses relations avec les dinoflagelles et sporozoaires. — Protistologica 15: 183–196.

    Google Scholar 

  • Buttner, D. W., 1967: Elektronmicroscopische Studien der Vermehrung von Theileria parva im Rind. — Z. Tropenmed. Parasit. 18: 245–268.

    CAS  Google Scholar 

  • — 1968: Vergleichende Untersuchung der Feinstruktur von Babesia gibsoni und Babesia canis. — Z. Tropenmed. Parasit. 19: 330–342.

    CAS  Google Scholar 

  • Bzik, D. J., 1991: The structure and role of RNA polymerases in Plasmodium. — Parasitol. Today 7: 211–214.

    PubMed  CAS  Google Scholar 

  • Cavalier-Smith, T., 1995a: Zooflagellate phylogeny and classification. — Cytology 37: 1010–1029.

    CAS  Google Scholar 

  • — 1995b: Membrane heredity, symbiogenesis, and the multiple origins of algae. — In Arai, R., Kato, M., Doi, Y., (Eds): Biodiversity and evolution, pp. 75–114. — Tokyo: National Science Museum.

    Google Scholar 

  • Couch, J., Thorsteinsen, K., Gilson, P., Deane, J., Hill, D., McFadden, G. I., 1996: Cryptomonad nuclear and nucleomorph 18S rRNA phylogeny. — Eur. J. Phycol. (in press).

    Google Scholar 

  • Cermakian, N., Ikeda, T. M., Cedergren, R., Gray, M. W., 1996: Sequences homologous to yeast mitochondrial and bacteriophage T3 and T7 RNA polymerases are widespread throughout the eukaryotic lineage. — Nucl. Acids. Res. 24: 648–654.

    PubMed  CAS  Google Scholar 

  • Colley, F. C., 1967: Fine structure of sporozoites of Eimeria nieschulzi. — J. Protozool. 14: 217–220.

    PubMed  CAS  Google Scholar 

  • Cook, G. C., 1995: Mefloquine toxicity should limit its use to treatment alone. — Brit. Med. J. 311: 190–191.

    PubMed  CAS  Google Scholar 

  • Creasey, A., Mendis, K., Carlton, J., Williamson, D., Wilson, I., Carter, R., 1994: Maternal inheritance of extrachromosomal DNA in malaria parasites. — Molec. Biochem. Parasitol. 65: 95–98.

    CAS  Google Scholar 

  • CyanoBase, 1996: The genome database for Synechocystis sp. strain PCC 6803 — http://www.kazusa.or.jp/cyano/cyano.html

    Google Scholar 

  • Dennis, D. T., 1989: Fatty acid biosynthesis in plastids. — In Boyer, C. D., Shannon, J. C., Hardison, R. C., (Eds): Physiology, biochemistry, and genetics of nongreen plastids, pp. 120–129 — Rockville: The American Society of Plant Physiologists.

    Google Scholar 

  • Miernyk, J. A., 1982: Compartmentation of nonphotosynthetic carbohydrate metabolism. — Annu Rev. Pl. Physiol. 33: 27–50.

    Google Scholar 

  • De Pamphilis, C. W., Palmer, J. D., 1989: Evolution and function of plastid DNA: a review with special reference to nonphotosynthetic plants. — In Boyer, C. D., Shannon, J. C., Hardison, R. C., (Eds): Physiology, biochemistry, and genetics of nongreen plastids, pp. 182–202. — Rockville: The American Society of Plant Physiologists.

    Google Scholar 

  • — 1990: Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. — Nature 348: 337–339.

    Google Scholar 

  • Doolan, D. L., Good, M. F., 1993: Develo** a malaria sporozoite vaccine. — Today’s Life Science 5: 18–19.

    Google Scholar 

  • Dore, E., Frontali, C., Forte, T., Fratarcangeli, S., 1983: Further studies and electron microscopic characterization of Plasmodium berghei DNA. — Molec. Biochem. Parasitol. 8: 339–352.

    CAS  Google Scholar 

  • Douce, R., Alban, C., Journet, E.-P., Joyard, J., 1989: Biochemical properties of plastids isolated from cauliflower buds and sycamore cells and of their envelope membranes. — In Boyer, C. D., Shannon, J. C., Hardison, R. C., (Eds): Physiology, biochemistry, and genetics of nongreen plastids, pp. 99–119. Rockville: The American Society of Plant Physiologists.

    Google Scholar 

  • Douglas, S. E., 1994: Chloroplast origins and evolution. — In Bryant, D. A., (Ed.): The molecular biology of Cyanobacteria, pp. 97–118. Dordrecht: Kluwer Academic Press.

    Google Scholar 

  • Dubremetz, J. F., 1995: Toxoplasma gondii: cell biology update. — In Boothroyd, J. C., Komuniecki, R. (Ed.): Molecular approaches to parasitology, pp. 345–358. — New York: Wiley-Liss.

    Google Scholar 

  • Egea, N., Lang-Unnasch, N., 1995: Phylogeny of the large extrachromosomal DNA of organisms in the phylum Apicomplexa. — J. Euk. Microbiol. 42: 679–684.

    PubMed  CAS  Google Scholar 

  • Escalante, A. A., Ayala, F. J., 1995:. Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes. — Proc. Natl. Acad. Sci. USA 92: 5793–5797.

    PubMed  CAS  Google Scholar 

  • Feagin, J. E., 1992: The 6 kb element of Plasmodium falciparum encodes mitochondrial cytochrome genes. — Molec. Biochem. Parasitol. 52: 145–148.

    CAS  Google Scholar 

  • — 1994: The extrachromosomal DNAs of apicomplexan parasites. — Annu. Rev. Microbiol. 48: 81–104.

    PubMed  CAS  Google Scholar 

  • — 1995: Exploring the organelle genomes of malaria parasites — In Boothroyd, J. C., Komuniecki, R. (Eds): Molecular approaches to parasitology, pp. 163–177. — New York: Wiley-Liss.

    Google Scholar 

  • Drew, M. E., 1995: Plasmodium falciparum: alterations in organelle transcript abundance during the erythrocytic cycle. — Exper. Parasitol. 80: 430–440.

    Google Scholar 

  • Gardner, M. J., Williamson, D. H., Wilson, R. J., 1991: The putative mitochondrial genome of Plasmodium falciparum. — J. Protozool. 38: 243–245.

    Google Scholar 

  • Werner, E., Gardner, M. J., Williamson, D. H., Wilson, R. J., 1992: Homologies between the contiguous and fragmented rRNAs of the two Plasmodium falciparum extrachromosomal DNAs are limited to core sequences. — Nucl. Acids Res. 20: 879–887.

    Google Scholar 

  • Fraser, J. D., Gocayne, O., White, M. D., Adams, R. A., Clayton, R. D., Venter, C. J., 1995: The minimal gene complement of Mycoplasma genitalium. — Science 270: 397–403.

    PubMed  CAS  Google Scholar 

  • Fleischmann, R. D., Adams, M. D., White, O., Clayton, R. A., Kirkness, E. F., Kerlavage, A. R., Bult, C. J., Tomb, J. E, Dougherty, B. A., Merrick, J. M., Venter, C. J., 1995: Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. — Science 269: 496–512.

    PubMed  CAS  Google Scholar 

  • Foissner, W., Foissner, I., 1984: First record of an ectoparasitic flagellate on ciliates. — Protistologica 20: 635–648.

    Google Scholar 

  • Gagnon, S., Levesque, R. C., Sogin, M. L., Gajadhar, A. A., 1993: Molecular cloning, complete sequence of the small subunit ribosomal RNA coding region and phylogeny of Toxoplasma gondii. — Molec. Biochem. Parasitol. 60: 145–148.

    CAS  Google Scholar 

  • Gajadhar, A. A., Marquardt, W. C., Hall, R., Gunderson, J., Ariztia, C. E. V., Sogin, M. L., 1991: Ribosomal RNA sequences of Sarcocystis muris, Theileria annulata and Crypthecodinium cohnii reveal evolutionary relationships among apicomplexans, dinoflagellates, and ciliates. — Molec. Biochem. Parasitol. 45: 147–154.

    CAS  Google Scholar 

  • Gardner, M. J., Bates, P. A., Ling, I. T., Moore, D. J., McCready, S., Gunasekera, M. B. R., Wilson, R. J. M., Williamson, D. H., 1988: Mitochondrial DNA of the human malarial parasite Plasmodium falciparum. — Molec. Biochem. Parasitol. 31: 11–18.

    CAS  Google Scholar 

  • Feagin, J. E., Moore, D. J., Spencer, D. F., Gray, M. W., Williamson, D. H., Wilson, R. J., 1991a: Organization and expression of small subunit ribosomal RNA genes encoded by a 35-kilobase circular DNA in Plasmodium falciparum. — Molec. Biochem. Parasitol. 48: 77–88.

    CAS  Google Scholar 

  • Williamson, D. H., Wilson, R. J. M., 1991b: A circular DNA in malaria parasites encodes an RNA polymerase like that of prokaryotes and chloroplasts. — Molec. Biochem. Parasitol. 44: 115–124.

    CAS  Google Scholar 

  • Feagin, J. E., Moore, D. J., Rangachari, K., Williamson, D. H., Wilson, R. J., 1993: Sequence and organization of large subunit rRNA genes from the extrachromosomal 35 kb circular DNA of the malaria parasite Plasmodium falciparum. — Nucl. Acids Res. 21: 1067–1071.

    PubMed  CAS  Google Scholar 

  • Preiser, P., Rangachari, K., Moore, D., Feagin, J. E., Williamson, D. H., Wilson, R. J., 1994a: Nine duplicated tRNA genes on the plastid-like DNA of the malaria parasite Plasmodium falciparum. — Gene 144: 307–308.

    PubMed  CAS  Google Scholar 

  • Goldman, N., Barnett, P., Moore, P. W., Rangachari, K., Strath, M., Whyte, A., Williamson, D. H., Wilson, R. J., 1994b: Phylogenetic analysis of the rpoB gene from the plastid-like DNA of Plasmodium falciparum. — Molec. Biochem. Parasitol. 66: 221–231.

    CAS  Google Scholar 

  • Goff, L. J., 1982: The biology of parasitic red algae. — Prog. Phycol. Res. 1: 289–369.

    Google Scholar 

  • Gozar, M.M.G., Bagnara, A. S., 1993: Identification of a Babesia bovis gene with homology to the small subunit ribosomal RNA gene from the 35-kilobase circular DNA of Plasmodium falciparum. — Int. J. parasitol. 23: 145–148.

    PubMed  CAS  Google Scholar 

  • — — 1995: 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. 25: 929–938.

    PubMed  CAS  Google Scholar 

  • Gray, M., 1992: Origin and evolution of organelle genomes. — Curr. Opinion Genet. Developm. 3: 884–890.

    Google Scholar 

  • Grimm, B., 1990: Primary structure of a key enzyme in plant tetrapyrrole synthesis: glutamate 1-semialdehyde aminotransferase. — Proc. Natl. Acad. Sci. USA 87: 4169–4173.

    PubMed  CAS  Google Scholar 

  • Hackstein, J. H., Mackenstedt, U., Mehlhorn, H., Meijerine, J. P., Schubert, H., Leunissen, J. A., 1995: Parasitic apicomplexans harbor a chlorophyll a-D1 complex, the potential target for therapeutic triazines. Parasitol. Res. 81: 207–216.

    PubMed  CAS  Google Scholar 

  • Harada, T., Ishikawa, R., Nizeki, M., Saito, K.-I., 1992: Pollen-derived rice calli that have larger deletions in plastid DNA do not require protein synthesis in plastids for growth. — Molec. Gen. Genet. 233: 145–150.

    PubMed  CAS  Google Scholar 

  • Harder, A., Haberkorn, A., 1989: Possible mode of action of toltrazuril: studies on two Eimeria species and mammalian and Ascaris suum enzymes. — Parasitol. Res. 76: 8–12.

    PubMed  CAS  Google Scholar 

  • Harris, E. H., Boynton, J. E., Gillham, N. W., 1994: Chloroplast ribosomes and protein synthesis. — Microbiol. Rev. 58: 700–754.

    PubMed  CAS  Google Scholar 

  • Hart, A. S., Ridigner, M. T., Soundarajan, R., Peters, C. S., Swiatlo, A. L., Kocka, F. E., 1990: Novel organism associated with chronic diarrhoea in AIDS. — Lancet 335: 169–170.

    PubMed  CAS  Google Scholar 

  • Hien, T. T., Day, N. P. J., Phu, N. H., Mai, N. T. H., Chau, T. T. H., Loc, P. P., Sinh, D. X., Chuong, L.V., Vinh, H., Waller, D., Peto, T. E. A., White, N. J., 1996: A controlled trial of artemether or quinine in Vietnamese adults with sever falciparum malaria. — New Engl. J. Med. 335: 76–83.

    CAS  Google Scholar 

  • Hoge, C. W., Shlim, D. R., Rajah, R., Triplett, J., Shear, M., Rabold, J. G., Echeverria, P., 1993: Epidemiology of diarrhoeal illness associated with coccidian-like organism among travellers and foreign residents in Nepal. — Lancet 341: 1175–1179.

    PubMed  CAS  Google Scholar 

  • Howe, C. J., 1992: Plastid origin of an extrachromosomal DNA molecule from Plasmodium, the causative agent of malaria. — J. Theor. Biol. 158: 199–205.

    PubMed  CAS  Google Scholar 

  • Smith, A. G., 1991: Plants without chlorophyll. — Nature 349: 109.

    Google Scholar 

  • Jeffries, A. C., Johnson, A. M., 1996: The growing importance of the plastid-like DNAs of the Apicomplexa. — Int. J. Parasitol. 26: 1139–1150.

    PubMed  CAS  Google Scholar 

  • Joseph, J. T., Aldritt, S. M., Unnasch, T., Puijalon, O., Wirth, D. E., 1989: Characterization of a conserved extrachromosomal element isolated from the avian malarial parasite Plasmodium gallinaceum. — Molec. Cell. Biol. 9: 3621–3629.

    PubMed  CAS  Google Scholar 

  • Kannangara, C. G., Gough, S. P., Bruyant, P., Hoober, J. K., Kahn, A., Wettstein, D. V., 1988: tRNAGlu as a cofactor in δ-aminolevulinate biosynthesis: steps that regulate chlorophyll synthesis. — Trends Biochem. Sci. 13: 139–143.

    PubMed  CAS  Google Scholar 

  • Kaplan, W., 1978: Protothecosis and infections caused by morphologically similar green algae. — Pan American Health Organization Scientific Publication 356: 218–232.

    Google Scholar 

  • Keeling, P. J., R. L., Doolittle, W. F., 1996: Alpha-tubulin from early diverging eukaryotic lineages and the evolution of the tubulin family. — Molec. Biol. Evol. 13: 1297–1305.

    PubMed  CAS  Google Scholar 

  • Charlebois, R. L., Doolittle, W. F., 1994: Archaebacterial genomes: eubacterial form and eukaryotic content. — Curr. Biol. 4: 816–822.

    CAS  Google Scholar 

  • Kepka, O., Scholtyseck, E., 1970: Weitere Untersuchungen der Feinstruktur von Frenkelia spec. (=M-Organismus, Sporozoa). — Protistologica 6: 249–266.

    Google Scholar 

  • Kilejian, A., 1975: Circular mitochondrial DNA from the avian malarial parasite Plasmodium lophurae. — Biochim. Biophys. Acta 390: 276–284.

    PubMed  CAS  Google Scholar 

  • Kleinschuster, S. J., Perkins, F. O., Dykstra, M. J., Swink, S. L., 1994: The in vitro life cycle of a Perkinsus species (Apicomplexa, Perkinsidae) isolated from Macoma balthica (Linneaus 1758). — J. Shellfish Res. 13: 461–465.

    Google Scholar 

  • Konishi, T., Sasaki, Y., 1994: Compartmentalization of two forms of acetyl-CoA carboxylase in plants and the origin of their tolerance towards herbicides. — Proc. Natl. Acad. Sci. USA 91: 3598–3601.

    PubMed  CAS  Google Scholar 

  • Kowallik, K. V., Stoebe, B., Schaffran, I., Kroth-Pancic, P., Freier, U., 1995: The chloroplast genome of a chlorophyll a + c containing alga, Odontella sinensis. — Pl. Molec. Biol. Reporter 13: 336–342.

    CAS  Google Scholar 

  • Kuijt, J., 1996: The biology of parasitic flowering plants. Berkeley: University of California Press.

    Google Scholar 

  • Kumar, S., Rzhetsky, A., 1996: Evolutionary relationships of eukaryotic kingdoms. — J. Molec. Evol. 42: 183–193.

    PubMed  CAS  Google Scholar 

  • Lea, P. J., Mills, W. R., Wallsgrove, R. M., Miflin, B. J., 1989: Assimilation of nitrogen and synthesis of amino acids in chloroplasts and cyanobacteria (blue-green algae). — In Schiff, J. A., (Ed.): On the origins of chloroplasts, pp. 149–178. — Amsterdam: Elsevier North Holland.

    Google Scholar 

  • Levine, N. P., 1988: The protozoan phylum Apicomplexa. — Boca Raton: CRC Press.

    Google Scholar 

  • Lim, S. H., Witty, M., Wallace, C. A. D. M., Ilag, L. I., Smith, A. G., 1994: Porphobilinogen deaminase is encoded by a single gene in Arbidopsis thaliana and is targeted to the chloroplasts. — Pl. Molec. Biol. 26: 863–872.

    CAS  Google Scholar 

  • Lindsay, D. S., Rippey, N. S., Toivio-Kinnucan, M. A., Blagburn, B. L., 1995: Ultrastructural effects of diclazuril against Toxoplasma gondii and investigations of a diclazuril-resistant mutant. — J. Parasitol. 81: 459–466.

    PubMed  CAS  Google Scholar 

  • Long, E. G., White, E. H., Carmichael, W. W., Quinslisk, P. M., Raja, R., Swisher, B. L., Daugharty, H., Cohen, M. T., 1991: Morphologic and staining characteristics of a cyanobacterium-like organism associated with diarrhea. — J. Infect. Dis. 164: 199–202.

    PubMed  CAS  Google Scholar 

  • Ebrahimzadeh, A., White, E. H., Swisher, B. L., Callaway, C. S., 1990: Alga associated with diarrhea in patients with acquired immunodeficiency syndrome and in travelers. — J. Clin. Microbiol. 28: 1101–1104.

    PubMed  CAS  Google Scholar 

  • MacDonald, C. M., Darbyshire, J. F., 1977: The morphology of a soil flagellate, Spiromonas angsta (Du.) Alexeieff (Mastigophorea: Protozoa). — Protistologica 13: 441–150.

    Google Scholar 

  • McConkey, G. A., Rogers, M. J., McCutchan, T. F., 1997: Inhibition of Plasmodium falciparum protein synthesis: targeting the plastid-like organelle with thiostreptin. — J. Biol. Chem. (in press).

    Google Scholar 

  • McFadden, G., 1991: Molecular cytology goes ultrastructural. — In Hall, J., Hawes, C., (Eds): Electron microscopy of plant cells, pp. 219–255. — London: Academic Press.

    Google Scholar 

  • — 1993: Second-hand chloroplasts: evolution of cryptomonad algae. — Adv. Bot. Res. 19: 189–230.

    Google Scholar 

  • Gilson, P., 1995: Something borrowed, something green: lateral transfer of chloroplasts by secondary endosymbiosis. — Trends Ecol. Evol. 10: 12–17.

    Google Scholar 

  • — — Hill, D., 1994: Goniomonas: rRNA sequences indicate that this phagotrophic flagellate is a close relative of the host component of cryptomonads. — Eur. J. Phycol. 29: 29–32.

    Google Scholar 

  • Reith, M. E., Mulholland, J., Lang-Unnasch, N., 1996: Plastid in human parasites. — Nature 381: 482.

    Google Scholar 

  • Melhorn, H., Schein, E., 1984: The Piroplasms: life cycle and sexual stages. — Adv. Parasitol. 23: 37–103.

    Google Scholar 

  • Ortmann-Flakenstein, G., Haberkorn, A., 1984: The effects of sym. triazines on development of Eimeria temila, E. maxima and E. acervulina: a light and electron microscopical study. — Z. Parasitenk. 70: 173–182.

    Google Scholar 

  • Mock, H. P., Trainotti, L., Kruse, E., Grimm, B., 1995: Isolation, sequencing and expression of cDNA sequences encoding uroporphyrinogen decarboxylase from tobacco and barley. — Pl. Molec. Biol. 28: 245–256.

    CAS  Google Scholar 

  • Myl’nikov, A. P., 1991: Ultrastructure and biology of certain representatives of the order Spiromonadida (Protozoa). — Zool. Zhurn. 7: 5–15.

    Google Scholar 

  • Nelissen, J., van de Peer, Y., Wilmotte, A., Wachter, R. D., 1995: An early origin of plastids within the cyanobacterial divergence is suggested by evolutionary trees based on complete 16S rRNA sequences. — Molec. Biol. Evol. 12: 1166–1173.

    PubMed  CAS  Google Scholar 

  • Ogino, N., Yoneda, C., 1996: The fine structure and mode of division of Toxoplasma gondii. — Arch. Ophthal. 75: 218–227.

    Google Scholar 

  • Olliaro, P. L., Goldberg, D. E., 1995: The Plasmodium digestive vacuole: metabolic headquarters and choice drug target. — Parasitol. Today 11: 294–297.

    PubMed  CAS  Google Scholar 

  • Ortega, Y. R., Sterling, C. R., Gilman, R. H., Cama, V. A., Diaz, F., 1993: Cyclospora species-new protozoan pathogen of humans. — New Engl. J. Med. 328: 1308–1312.

    PubMed  CAS  Google Scholar 

  • Palmer, J. D., 1992a: Green ancestry of malarial parasites? — Curr. Biol. 2: 318–320.

    PubMed  CAS  Google Scholar 

  • — 1992b: Comparison of chloroplasts and mitochondrial genome evolution in plants. — In Hermann, H., (Ed.): Plant gene research. Cell organelles, pp. 137–163. — Wien: Springer.

    Google Scholar 

  • Delwiche, C. F., 1996: Second-hand chloroplasts and the case of the disappearing nucleus. — Proc. Natl. Acad. Sci. USA 93: 7432–7435.

    Google Scholar 

  • Pawlovskki, J., Bolivar, I., Fahrni, J. F., Cavalier-Smith, T., Gouy, M., 1996: Early origin of foraminifera suggested by SSU rRNA gene sequences. — Molec. Biol. Evol. 13: 445–450.

    Google Scholar 

  • Perkins, F. O., 1969: Ultrastructure of vegetative stages in Labyrinthomyxa marina (=Dermocystidium marinum), a commercially significant oyster pathogen. — J. Invert. Pathol. 13: 199–222.

    CAS  Google Scholar 

  • — 1976: Zoospores of the oyster pathogen, Dermocystidium marinum. I. Fine structure of the conoid and other sporozoan-like organelles — J. Parasitol. 62: 959–974.

    Google Scholar 

  • Menzel, R.W., 1967: Ultrastructure of sporulation in the oyster pathogen Dermocystidium marinum. — J. Invert. Pathol. 9: 205–229.

    Google Scholar 

  • Pietrokovski, S., 1994: Conserved sequence feature of inteins (protein introns) and their use in identifying new inteins and related proteins. — Protein Sci. 3: 2340–2350.

    PubMed  CAS  Google Scholar 

  • Porchet-Hennere, E., 1972: Observations en mictoscopie photonique et electronique sur la sporogenese de Dehornia (1) sthenelais (n. gen., sp. n.), sporozoaire parasite de I’annelide polychete Sthenelais boa (Aphroditides). — Protistologica 8: 245–255.

    Google Scholar 

  • Richard, A., 1970: Ultrastructure des stades végétatifs d’ Aggregata eberthi Labbé: le trophozoite et le schizonte. — Z. Zeilforsch. 103: 179–191.

    Google Scholar 

  • Preiser, P., Williamson, D. H., Wilson, R. J., 1995: tRNA genes transcribed from the plastid-like DNA of Plasmodium falciparum. — Nucl. Acids Res. 23: 4329–4336.

    PubMed  CAS  Google Scholar 

  • Pukrittayakamee, S., Viravan, C., Charoenlarp, P., Yeamput, C., Wilson, R. J., White, N. J., 1994: Antimalarial effects of rifampin in Plasmodium vivax malaria. — Antimicrob. Agents Chemother. 38: 511–514.

    PubMed  CAS  Google Scholar 

  • Radchenko, A. I., 1987: Sarcocystis muris (Sporozoa, Apicomplexa): the mode of division of the intermediate cell in the cyst as revealed by electron microscope. — Tsitologiia 29: 404–409.

    PubMed  CAS  Google Scholar 

  • Raventos-Suarez, C., Pollack, S., Nagel, R., 1982: Plasmodium falciparum: inhibition of in vitro growth by desferrixamine. — Amer. J. Trop. Med. Hyg. 31: 919–922.

    CAS  Google Scholar 

  • Reardon, E. M., Price, C. A., 1995: Plastid genomes of three non-green algae are sequenced. — Pl. Molec. Biol. Reporter 13: 320–326.

    Google Scholar 

  • Turano, F. J., Weisemann, J. M., Wilson, B. J., Matthews, B. F., 1989: Amino acid biosynthesis and nitrogen assimilation in higher plants. In: Boyer, C. D., Shannon, J. C., Hardison, R. C., (Eds.): Physiology, biochemistry, and genetics of nongreen plastids, pp. 130–140. — Rockville: The American Society of Plant Physiologists.

    Google Scholar 

  • Reith, M. E., Munholland, J., 1993: A high resolution gene map of the chloroplast genome of the red alga Porphyra purpurea. — Pl. Cell 5: 465–475.

    CAS  Google Scholar 

  • Relman, D. A., Schmidt, T. M., Garjadar, A., Sogin, M., Cross, J., Yoder, K., Sehtabutr, O., Echeverria, P., 1996: Molecular phylogenetic analysis of Cyclospora, the human intestinal pathogen, suggests that it is closely related to Eimeria species. — J. Infect. Dis. 173: 440–445.

    PubMed  CAS  Google Scholar 

  • Roberts, W. L., Hammond, D. M., Anderson, L. C., Speer, C. A., 1970: Ultrastructural study of schizogony in Eimeria callospermophili and E. Iarmerensis. — J. Protozool. 17: 584–592.

    PubMed  CAS  Google Scholar 

  • Rudzinska, M. A., Trager, W., 1962: Intracellular phagotrophy in Babesia rodhaini as revealed by electron microscopy. — J. Protozool. 9: 279–288.

    PubMed  CAS  Google Scholar 

  • Vickerman, K., 1968: The fine structure — In Weinman, D., Ristic, M., (Eds): Infectious blood diseases of man and animals: Diseases caused by Protista. I, pp. 217–306. — New York: Academic Press.

    Google Scholar 

  • Rush, M. G., Misra, R., 1985: Extrachromosomal DNA in eukaryotes. — Plasmid 14: 177–191.

    PubMed  CAS  Google Scholar 

  • Sadler, L. A., McNally, K. L., Govind, N. S., Brunk, C. F., Trench, R. K., 1992: The nucleotide sequence of the small subunit ribosomal RNA gene from Symbiodinium pilosum, a symbiotic dinoflagellate. — Curr. Genet. 21: 409–416.

    PubMed  CAS  Google Scholar 

  • Scholtyseck, E., 1979: Fine structure of the parasitic protozoa: an atlas of micrographs, drawings and diagrams. — Berlin: Springer.

    Google Scholar 

  • Piekarski, G. P., 1965: Electronenmikroscopische Untersuchungen an Merozoiten von Eimerien (Eimeria performs und E. stiedae) und Toxoplama gondii zur systematischen Stellung von T. gondii. — Z. Parasiten. 26: 91–115.

    Google Scholar 

  • Schrevel, J., 1971: Contribution a l’étude des Selenidiidae parasites d’annélides polychétes II. ultrastructure de quelques trophozoites. Protistologica 7: 101–130.

    Google Scholar 

  • Sheffield, H. G., 1966: Electron microscope study of the proliferative form of Besnoitia jellisoni. — J. Parasitol. 52: 583–594.

    PubMed  CAS  Google Scholar 

  • Melton, M. L., 1968: The fine structure and reproduction of Toxoplasma gondii. — J. Parasitol. 54: 209–226.

    Google Scholar 

  • Seddall, M. E., 1992: Hohlzylinders. — Parasitol. Today 8: 90–91.

    Google Scholar 

  • Stokes, N. A., Burreson, E. M., 1995: Molecular phylogenetic evidence that the phylum Haplosporida has an alveolate ancestry. — Molec. Biol. Evol. 12: 573–581.

    Google Scholar 

  • Silberman, J. D., Sogin, M. L., Leipe, D. D., Clark, C. G., 1996: Human parasite finds taxonomic home. — Nature 380: 398.

    PubMed  CAS  Google Scholar 

  • Simpson, A. F. B., Patterson, D. J., 1996: Ultrastructure and identification of the predatory flagellate Colpodella pugnax Cienkowski (Apiconiplexa) with a description of Colpodella turpis n. sp. and a review of the genus. — Syst. Parasitol. 33: 187–198.

    Google Scholar 

  • Slater, A. F. G., Cerami, A., 1992: Inhibition by chloroquine of a novel haem polymerase enzyme activity in malaria trophozoites. — Nature 355: 167–169.

    PubMed  CAS  Google Scholar 

  • Small, I., Suffolk, R., Leaver, C. J., 1989: Evolution of plant mitochondrial genomes via substoichiometric intermediates. — Cell 58: 69–76.

    PubMed  CAS  Google Scholar 

  • Sterling, C., De Giusti, D., 1972: Ultrastructural aspects of schizogony, mature schizonts, and merozoites of Haemoproteus metchnikovi. — J. Parasitol. 58: 641–652.

    PubMed  CAS  Google Scholar 

  • Strath, M., Scott, F. T., Gardner, M., Williamson, D., Wilson, I., 1993: Antimalarial activity of rifampicin in vitro and in rodent models. — Trans Roy. Soc. Trop. Med. Hyg. 87:211–216.

    PubMed  CAS  Google Scholar 

  • Surolia, N., Padmanaban, G., 1992: De novo biosynthesis of heme offers a new chemotherapeutic target in the human malarial parasite. — Biochem. Biophys. Res Com. 187: 744–750.

    PubMed  CAS  Google Scholar 

  • Taylor, E J. R., 1990: Phylum Dinoflagellata. — In Margulis, L., Corliss, J. O., Melkonian, M., Chapman, D. J., (Eds): Handbook of Protoctista, pp. 549–573.-Boston: Jones & Bartlett.

    Google Scholar 

  • Vaidya, A. B., Akella, R., Suplick, K., 1989: Sequences similar to genes for two mitochondrial proteins and portions of ribosomal RNA in tandemly arrayed 6-kilobasepair DNA of a malarial parasite. — Molec. Biochem. Parasitol. 35: 97–108.

    CAS  Google Scholar 

  • Vanhensbroek, M. B., Onyiorah, E., Jaffar, S., Schneider, G., Palmer, A., Frenkel, J., Enwere, G., Forck, S., Nusmeijer, A., Bennett, S., Greenwood, B., Kwiatkowski, D., 1996: A trial of arthemeeter or quinine in children with cerebral malaria. — New Engl. J. Med. 335: 69–75.

    CAS  Google Scholar 

  • Van de Peer, Y., Rensing, S., Maier, U.-G., Wachter, R. D., 1996: Substitution rate calibration of small subunit rRNA identifies chlorarachniophyte endosymbionts as remnants of green algae. — Proc. Natl. Acad. Sci. USA 93: 7732–7736.

    PubMed  Google Scholar 

  • Van der Zypen, E., Piekarski, G., 1967: Ultrastrukturelle Unterschiede zwischen der sog. Proliferationsform (RH-Stamm, BK-Stamm) und dem sog. Cysten-Stadium (DX-Stamm) von Toxoplasma gondii. Zentralbl. Bakteriol. Parasitenk. 203: 495–517.

    Google Scholar 

  • Vivier, E., Desportes, I., 1990: Apicomplexa. — In Margulis, L., Corliss, J. O., Melkonian, M., Chapman, D. J., (Eds): Handbook of Protoctista, pp. 549–573. — Boston: Jones & Bartlett.

    Google Scholar 

  • Hennere, E., 1965: Ultrastructure des stades végétatifs de la coccidie Coelotropha durchoni. — Protistologica 1: 89–104.

    Google Scholar 

  • Petitprez, A., 1969: Observations ultrastructurales sur l’hématozoaire Anthesoma garnhami et examen de critères morphologiques utilisables pour la taxonomie chez les sporozoaires. — Protistologica 5: 363–379.

    Google Scholar 

  • Petitprez, A., Landau, I., 1972: Observations ultrastructurales sur la sporoblastogenése de I’hémogregarine, Hepatozoon domerguei, Coccide Adeleidea. — Protistologica 8: 315–334.

    Google Scholar 

  • Walsh, M. A., Rechel, E. A., Popovich, T. M., 1980: Observations of plastid fine structure in the holoparasitic angiosperm Epifagus virginiana. — Amer. J. Bot. 67: 833–837.

    Google Scholar 

  • Whatley, J. M., 1977: Variation in the basic pathway of chloroplast development. — New Phytol. 78: 407–420.

    Google Scholar 

  • Wildführ, W., 1966: Elektronenmikroskopische Untersuchungen zur Morphologie and Reproduktion von Toxoplama gondii. — Zentralbl Bakteriol. I. Abt. orig. 201: 110–130.

    Google Scholar 

  • Williamson, D. H., Wilson, R. J. M., Bates, R. A., McCready, S., Perler, R., Qiang, B.-U., 1985: Nuclear and mitochondrial DNA of the primate parasite Plasmodium knowlesi. — Molec. Biochem. Parasitol. 14: 199–209.

    CAS  Google Scholar 

  • Gardner, M. J., Preisher, P., Moore, D. J., Rangachari, K., Wilson, R. J. M., 1994: The evolutionary origin of the 35 kb circular DNA of Plasmodium falciparum: new evidence supports a possible rhodophyte ancestry. — Molec. Gen. Genet. 243: 249–252.

    PubMed  CAS  Google Scholar 

  • Preiser, P., Wilson, R. J. M., 1996: Organelle DNAs: the bit players in malaria parasite DNA replication. — Parasitol. Today 12: 357–362.

    PubMed  CAS  Google Scholar 

  • Wilson, C. M., Smith, A.B., Baylon, R. V., 1996: Characterization of the deltaaminolevulinate synthase gene homologue in Plasmodium falciparum. — Molec. Biochem. Parasitol. 75: 271–275.

    CAS  Google Scholar 

  • Wilson, I., 1993: Plastids better red than dead. — Nature 366: 638.

    PubMed  CAS  Google Scholar 

  • Wilson, R. J. M., Gardner, M. J., Feagin, J. E., Williamson, D. H., 1991: Have malaria parasites three genomes? — Parasitol. Today 7: 134–136.

    PubMed  CAS  Google Scholar 

  • Fry, M., Gardner, M. J., Feagin, J. E., Williamson, D. H., 1992: Subcellular fractionation of the two organelle DNAs of malaria parasites — Curr. Genet. 21: 405–408.

    Google Scholar 

  • Gardner, M. J., Rangachari, K., Williamson, D. H., 1993: Extrachromosomal DNAs in the Apicomplexa. — In Smith, J. E., (Ed.): Toxoplasmosis, NATO ASI Series H78: 51–60. — Berlin: Springer.

    Google Scholar 

  • Denny, R W., Preisser, R R., Rangachari, K., Roberts, K., Roy, A., Whyte, A., Strath, M., Moore, D. J., Moore, R W., Williamson, D. H., 1996: Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. — J. Molec. Biol. 261: 155–172.

    PubMed  CAS  Google Scholar 

  • Williamson, D. H., Preiser, P., 1994: Malaria and other Apicomplexans: the “plant” connection. — Infect. Agents Disease 3: 29–37.

    CAS  Google Scholar 

  • Wolfe, K. H., Morden, C. W., Palmer, J., 1992: Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc. Natl. Acad. Sci. USA 89: 10648–10652.

    PubMed  CAS  Google Scholar 

  • Wolters, J., 1991: The troublesome parasites: Molecular and morphological evidence that Apicomplexa belong to the dinoflagellate-ciliate clade. — BioSystems 25: 75–84.

    PubMed  CAS  Google Scholar 

  • Woods, K. M., Nesterenko, M. V., Upton, S. J., 1996: Efficacy of 101 antimicrobials and other agents on the development of Cryptosporidium parvum in vitro. — Ann. Trop. Med. Parasitol. 90: 603–615.

    PubMed  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1997 Springer-Verlag Wien

About this chapter

Cite this chapter

Mcfadden, G.I., Waller, R.F., Reith, M.E., Lang-Unnasch, N. (1997). Plastids in apicomplexan parasites. In: Bhattacharya, D. (eds) Origins of Algae and their Plastids. Plant Systematics and Evolution, vol 11. Springer, Vienna. https://doi.org/10.1007/978-3-7091-6542-3_14

Download citation

  • DOI: https://doi.org/10.1007/978-3-7091-6542-3_14

  • Publisher Name: Springer, Vienna

  • Print ISBN: 978-3-211-83035-2

  • Online ISBN: 978-3-7091-6542-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Navigation