Skip to main content
SpringerLink
Log in

The Origin, Losses and Gains of Chloroplasts

  • Chapter
Origins of Plastids

Summary

Chloroplasts originated, probably once only, from a symbiotic cyanobacterium about 700–900 million years ago, and subsequently diversified in pigmentation, in patterns of thylakoid stacking, and in envelope structure, to produce all the major types of eukaryotic algae. Dinoflagellates and the two subkingdoms [Viridiplantae (green plants) and Biliphyta (red algae and glaucophytes)] of the kingdom Plantae probably diverged directly from a phagotrophic Cyanophoral Colponema-like biflagellate protozoan that already had a chloroplast. During the same epoch two independent lateral transfers of some of these early diverging chloroplasts (and of nuclear genes coding for some of their proteins) occurred by the endosymbiotic merger of two eukaryote cells. These secondary symbioses yielded one major predominantly photosynthetic taxon, the kingdom Chromista, and a minor algal class (Chlorarachnea) containing only the green reticulate amoeboflagellate genus Chlorarachnion. It has been suggested that the green chloroplasts of Euglena and the other members of the euglenoid class Euglenophyceae also arose by a secondary symbiosis involving a eukaryotic alga (possibly a green alga). However, more and more evidence supports the alternative view that no secondary symbiosis was involved, and that the euglenoid chloroplast is simply the earliest diverging of all and arose directly from the same cyanobacterium as all other chloroplasts. The prochlorobacteria (Prochloron, Prochlorothrix and Prochlorococcus) are cyanobacterial derivatives not specifically related either to green plant or to euglenoid chloroplasts, and are probably not even a monophyletic group: chlorophyll b probably evolved 4 times independently, thrice in photosynthetic bacteria and once in chloroplasts. Photosynthesis has been frequently lost by both bacteria and eukaryotes. However plastids have probably never been lost by plants, but have been lost (rarely: at least thrice) by chromists and (frequently: at least 30 times) by dinoflagellates. How often they have been lost by euglenoids is unclear. I propose that they were also lost, independently, by at least one protalveolate dinozoan flagellate, the ancestor of extant protalveolates (e.g. Colponema) and of Ciliophora and Apicomplexa, and by the ancestral opalozoan flagellate, from which most other non-photosynthetic protozoa including the choanoflagellate ancestors of animals and fungi probably evolved. I propose that chloroplasts originated in a tetrakont protozoan host, from which a biflagellate photo-phagotrophic lineage evolved that very soon gave rise to the euglenoids and other euglenozoa on the one hand and to the photo-phagotrophic common ancestor of the Dinozoa (dinoflagellates plus Protalveolata), the Plantae, and the Opalozoa on the other. I suggest that the symbiotic origin of chloroplasts directly stimulated the origin of Golgi dictyosomes, and of several other relatively advanced eukaryotic features including nuclear spliceosomal introns and the trans-splicing of 5’ mini-exons in Euglenozoa. The evidence and reasons for these conclusions are outlined.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

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.

References

  • Aitken, A. and R.Y. Stanier. 1979. Characterization of peptidoglycan from the cyanelles of Cyanophora paradoxa. J. Gen. Microbiol. 112:219–223.

    Article  CAS  Google Scholar 

  • Allen, J.F., N.G. Holmes, C.W. Mullineaux, and C.E. Sanders. 1986. More on thylakoid membrane stacking. Trends Biochem. Sci. 11:320.

    Article  CAS  Google Scholar 

  • Bhattacharya, D., H.J. Elwood, L.J. Goff, and M.L. Sogin. 1990. Phylogeny of Gracilaria lemaneiformis (Rhodophyta) based on sequence analysis of its small subunit ribosomal RNA coding region. J. Phycol. 26:181–186.

    Article  CAS  Google Scholar 

  • Blobel, G. 1980. Intracellular protein topogenesis. Proc. Natl. Acad. Sci. USA 77:1496–1500.

    Article  PubMed  CAS  Google Scholar 

  • Brandes, D. 1965. Observations on the apparent mode of formation of pure lysosomes. J. Ultrastruct. Res. 12:63–80.

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith, T. 1978. The evolutionary origin and phylogeny of microtubules, mitotic spindles and eukaryote flagella. BioSystems 10:93–114.

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith, T. 1981a. Eukaryote kingdoms: seven or nine? BioSystems 14:461–481.

    Article  CAS  Google Scholar 

  • Cavalier-Smith, T. 1981b. The origin and early evolution of the eukaryote cell. p. 33–84. In: Molecular and Cellular Aspects of Microbial Evolution, M.J. Carlile, J.F. Collins, and B.E.B. Moseley (eds.). Society for General Microbiology Symposium 32. Cambridge University Press.

    Google Scholar 

  • Cavalier-Smith, T. 1982. The origins of plastids. BioL J. Linn. Soc. 17:289–306.

    Article  Google Scholar 

  • Cavalier-Smith, T. 1983. Endosymbiotic origin of the mitochondrial envelope. p. 265–279. In: Endocytobiology II,W. Schwemmler and H.E.A. Schenk (eds.). de Gruyter, Berlin.

    Google Scholar 

  • Cavalier-Smith, T. 1986. The kingdom Chromista: origin and systematics. pp. 309–347. In: Progress in Phycological Research, vol 4. F.E. Round and D.J. Chapman (eds.). Biopress Ltd., Bristol.

    Google Scholar 

  • Cavalier-Smith, T. 1987a. Glaucophyceae and the origin of plants. Evol. Trends Plants 2:75–78.

    Google Scholar 

  • Cavalier-Smith, T. 1987b. Bacterial DNA segregation: its motors and positional control. J. Theor. Biol. 127:361–372.

    Article  CAS  Google Scholar 

  • Cavalier-Smith, T. 1987c. The origin of fungi and pseudofungi. Symp. Brit. Mycol. Soc. 13:339–353. In: Evolutionary Biology of the Fungi, A.D.M. Rayner, C.M. Brasier, and D. Moore (eds.). Cambridge University Press.

    Google Scholar 

  • Cavalier-Smith, T. 1987d. The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies. Annu. NY Acad. Sci. 503:55–71.

    Article  CAS  Google Scholar 

  • Cavalier-Smith, T. 1987e. The origin of eukaryote and archaebacterial cells. Annu. NY Acad. Sci. 503:17–54.

    Article  CAS  Google Scholar 

  • Cavalier-Smith, T. 1989. The kingdom Chromista. p. 379–405. In: The Chromophyte Algae: Problems and Perspectives, J.C. Green, B.S.C. Leadbeater, and W.C. Diver (eds.). Oxford University Press.

    Google Scholar 

  • Cavalier-Smith, T. 1990a. Microorganism megaevolution: integrating the living and fossil evidence. Rev. Micropal. 33:145–154.

    Google Scholar 

  • Cavalier-Smith, T. 1990b. The symbiotic origin of peroxisomes. p. 515–521. In: Endocytobiology IV, P. Nardon, V. Gianinazzi-Pearson, A.M. Grenier, L. Margulis, and D.C. Smith (eds.). Institut National de la Recherche Agronomique, Paris.

    Google Scholar 

  • Cavalier-Smith, T. 1991a. The evolution of prokaryotic and eukaryotic cells. p. 217–272. In:Fundamentals of Medical Cell Biology,Vol. I, G.E. Bittar (ed.). J.A.I. Press, Greenwich, Connecticut.

    Google Scholar 

  • Cavalier-Smith, T. 1991b. The evolution of cells. p. 271–304. In: Evolution of Life. Proceedings of Congress of Institute for Advanced Research Conference at Kyoto, S. Osawa and T. Honjo (eds.). Springer-Verlag, Tokyo.

    Google Scholar 

  • Cavalier-Smith, T. 1991c. Intron phylogeny: A new hypothesis. Trends Genet. 7:145–148.

    Article  CAS  Google Scholar 

  • Cavalier-Smith, T. 1991d. Cell diversification in heterotrophic flagellates. p. 113–131. In: The Biology of Free-living Heterotrophic Flagellates, D.J. Patterson and J. Larsen (eds.). Clarendon Press, Oxford.

    Google Scholar 

  • Cavalier-Smith, T. 1991e. Archamoebae: the ancestral eukaryotes? BioSystems 24:25–38.

    Article  Google Scholar 

  • Cavalier-Smith, T. 1992a. Kingdom Protozoa and its 16 phyla. J. Protozool., In press. Cavalier-Smith, T. 1992b. The origin of chloroplasts and the kingdom Plantae. Adv. Bot. Res., In press.

    Google Scholar 

  • Cavalier-Smith, T. and J.J. Lee. 1985. Protozoa as hosts for endosymbioses and the conversion of symbionts into organelles. J. Protozool. 32:376–379.

    Google Scholar 

  • Dodge, J.D. 1985. A re-examination of the relationship between unicellular host and eucaryotic endosymbiont with special reference to Glenodinium foliaceum Dinophyceae. p. 1015–1026. In: Endocytobiology II, H.E.A. Schenk and W. Schwemmler (eds.). de Gruyter, Berlin.

    Google Scholar 

  • Douce, R. and J. Joyard. 1981. Does the plastid envelope derive from the endoplasmic reticulum? Trends Biochem. Sci. 6:237–239.

    Article  CAS  Google Scholar 

  • Dorne, A.-J., J. Joyard, M.A. Block, and R. Douce. 1985. Localization of phosphatidyicholine in outer envelope membrane of spinach chloroplasts. J. Cell Biol. 100:1690–1697.

    Article  PubMed  CAS  Google Scholar 

  • Dorne, A.-J., J. Joyard, and R. Douce. 1990. Do thylakoids really contain phosphatidylcholine? Proc. Natl. Acad. Sci. USA 87:71–74.

    Article  PubMed  CAS  Google Scholar 

  • Dougherty, E.C. and M.B. Allen. 1960. Is pigmentation a clue to protistan phylogeny? p. 129–144. In: Comparative Biochemistry of Photoreactive Systems, E.C. Dougherty and M.B. Allen (eds.). Academic Press, New York.

    Google Scholar 

  • Douglas, S.E., C.A. Murphy, D.F. Spencer, and M.W. Gray. 1991. Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350:148–151.

    Article  PubMed  CAS  Google Scholar 

  • Eschbach, S., C.J.B. Hofmann, U.-G. Maier, P. Sitte, and P. Hansmann. 1991. A eukaryotic genome of 660 kb: Electrophoretic karyotype of nucleomorph and cell nucleus of the cryptomonad alga, Pyrenomonas salina. Nucleic Acids Res. 19:1779–1781.

    Article  PubMed  CAS  Google Scholar 

  • Evrard, J.L., M. Kuntz, and J.H. Weil. 1990. The nucleotide sequence of five ribosomal protein genes from the cyanelles of Cyanophora paradoxa: implications concerning the phylogenetic relationship between cyanelles and chloroplasts. J. Mol. Evol. 30:16–25.

    Article  PubMed  CAS  Google Scholar 

  • Farmer, M.A. and R.E. Triemer. 1991. A taxonomic redescription of euglenoid flagellates based on ultrastructural characters. J. Phycol. 27:20.

    Google Scholar 

  • Gallo, J.-M. and J. Schrevel. 1985. Homologies between paraflagellar rod proteins from trypanosomes and euglenoids revealed by monoclonal antibody. Eur. J. Cell Biol. 36:163–168.

    PubMed  CAS  Google Scholar 

  • Gibbs, S.P. 1978. The chloroplasts of Euglena may have evolved from symbiotic green algae. Can. J. Bot. 56:2883–2889.

    Article  Google Scholar 

  • Gibbs, S.P. 1981. The chloroplast endoplasmic reticulum, structure, function, and evolutionary significance. Int. Rev. Cytol. 72:49–99.

    Article  Google Scholar 

  • Gillott, M.A. and S.P. Gibbs. 1980. The cryptomonad nucleomorph: its ultrastructure and evolutionary significance. J. Phycol. 16:558–568.

    Article  Google Scholar 

  • Gray, M.W. and W.F. Doolittle. 1982. Has the endosymbiont hypothesis been proven? Microbiol. Rev. 46:1–42.

    PubMed  CAS  Google Scholar 

  • Greenwood, A.D. 1974. The Cryptophyta in relation to phylogeny and photosynthesis. 8th International Congress of Electron Microscopy, Canberra.

    Google Scholar 

  • Grossman, A., A. Manodori, and D. Snyder. 1990. Light-harvesting proteins of diatoms — their relationship to the chlorophyll alb binding proteins of higher plants and their mode of transport into plastids. Mol. Gen. Genet. 224:91–100.

    Article  PubMed  CAS  Google Scholar 

  • Hansmann, P. and S. Eschbach. 1990. Isolation and preliminary characterization of the nucleus and the nucleomorph of a cryptomonad, Pyrenomonas salina. Eur. J. Cell Biol. 52:373–378.

    PubMed  CAS  Google Scholar 

  • Hendriks, L., R. De Baere, Y. van de Peer, J. Neefs, A. Goris, and R. De Wachter. 1991. The evolutionary position of the rhodophyte Porphyra umbilicalis and the basidiomycete Leucosporidium scottii among other eukaryotes as deduced from complete sequences of small ribosomal subunit RNA. J. Mol. Evol. 32:167–177.

    Article  PubMed  CAS  Google Scholar 

  • Herdman, M. and R.Y. Stanier. 1977. The cyanelle: chloroplast or endosymbiotic prokaryote? FEMS Lett. 1:7–12.

    Article  CAS  Google Scholar 

  • Hibberd, D.J. and R.E. Norris. 1984. Cytology and ultrastructure of Chlorarachnion reptans (Chlorarachniophyta divisio nova, Chlorarachniophyceae classis nova). J. Phycol. 20:310–330.

    Article  Google Scholar 

  • Höfeld, I., J. Otten, and M. Melkonian. 1988. Contractile eukaryote flagella: centrin is involved. Protoplasma 147:16–24.

    Article  Google Scholar 

  • Jeffrey, C. 1971. Thallophytes and kingdoms — a critique. Kew. Bull. 25:291–299.

    Article  Google Scholar 

  • Joyard, J., M.A. Block, A.-J. Dorne, and R. Douce. 1987. Comparison of envelope membranes from higher plants and algae plastids and of outer membranes from cyanobacteria (blue-green algae). p. 123–133. In: Algal Development (Molecular and Cellular Aspects). W. Wiesner, D.G. Robinson, and R.C. Starr (eds.). Springer-Verlag, Berlin.

    Google Scholar 

  • Kies, L. 1988. The effect of penicillin on the morphology and ultrastructure of Cyanophora, Gloeochaete and Glaucocystis (Glaucocystophyceae) and their cyanelles. Int. J. Endocytob. Cell Res. 5:361–372.

    Google Scholar 

  • Kivic, P.A. and P.L. Walne. 1984. An evaluation of a possible phylogenetic relationship between the Euglenophyta and Kinetoplastida. Origins Life 13:269–288.

    Article  Google Scholar 

  • Klein, R. and A. Cronquist. 1967. A consideration of the evolutionary and taxonomic significance of some biochemical, micromorphological and physiological characters in the Thallophytes. Q. Rev. Biol. 42:105–296.

    PubMed  CAS  Google Scholar 

  • Knoll, A.H. 1989. Evolution and extinction in the marine realm; some constraints imposed by the phytoplankton. Phil. Trans. Roy. Soc Lond. B, 325:229–290.

    Article  Google Scholar 

  • Lahti, C.J. and P.J. Johnson. 1991. Trichomonas vaginalis hydrogenosomal proteins are synthesised on free polyribosomes and may undergo processing upon maturation. Mol. Biochem. Parasitol. 46:307–310.

    Article  PubMed  CAS  Google Scholar 

  • Lambert, D.H., D.A. Bryant, V.L. Stirewalt, J.M. Dubbs, S.E. Stevens, and R.D. Porter. 1985. Gene map for the Cyanophora paradoxa cyanelle genome. J. Bacteriol. 164:659–664.

    PubMed  CAS  Google Scholar 

  • Larouche, L., C. Tremblay, C. Simard, and G. Belleneve. 1991. Characterization of a cDNA encoding a PSII-associated chlorophyll alb binding protein (Cab) from Chlamydomonas moewusii fitting into neither type I nor type II. Curr. Genet. 19:285–288.

    Article  PubMed  CAS  Google Scholar 

  • Lauterborn, R. 1895. Protozoenstudien. II. Paulinella chromatophora nov. gen., nov. spec., ein beschalter Rhizopode des Süsswassers mit blaugrünen chromatophoren-artigen Einschlüssen. Z. Wiss. Zool. 59:537–544.

    Google Scholar 

  • Lefort-Tran, M. 1981. The triple layered organization of the Euglena chloroplast envelope (signification and functions). Ber. D. Tsch. Bot. Ges. 94:463–476.

    Google Scholar 

  • Lewin, R.A. and L. Cheng. 1989. Prochloron: A Microbial Enigma. Chapman Hall, New York.

    Book  Google Scholar 

  • Li, C.-W. and B.E. Volcani. 1987. Four new apochlorotic diatoms. Br. Phycol. J. 22:375–382.

    Article  Google Scholar 

  • Lonsdale, D.M., T.P. Hodge, C.J. Howe, and D.B. Stern. 1983. Maize mitochondrial DNA contains a sequence homologous to the ribulose-1,5 bisphosphate carboxylase large subunit gene of chloroplast DNA. Cell 34:1007–1014.

    Article  PubMed  CAS  Google Scholar 

  • Ludwig, M. and S.P. Gibbs. 1985. DNA is present in the nucleomorph of cryptomonads: further evidence that the chloroplast evolved from a eukaryotic endosymbiont. Protoplasma 127:9–20.

    Article  Google Scholar 

  • Manodori, A. and A.R. Grossman. 1990. Sequence homology between light harvesting polypeptides of plants and the diatom Phaeodactylum tricornutum. Vol. III, p. 541–544. In: Current Research in Photosynthesis, M. Baltscheffsky (ed.). Kluwer, Dordrecht.

    Google Scholar 

  • Margulis, L. 1970. Origin of Eukaryotic Cells. Yale University Press, New Haven.

    Google Scholar 

  • Margulis, L. 1981. Symbiosis in Cell Evolution. Freeman, San Francisco.

    Google Scholar 

  • Margulis, L. and R. Obar. 1985. Heliobacterium and the origin of chrysoplasts. BioSystems 17:317–325.

    Article  PubMed  CAS  Google Scholar 

  • Matsubayashi, T., T. Wakasugi, K. Shinozaki, K. Yamaguchi-Shinozaki, N. Zaita, T. Hidaka, B. Y. Meng, C. Ohto, M. Tanaka, A. Kato, T. Maruyama, and M. Sugiura. 1987. Six chloroplast genes (ndhA-F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenose are actively expressed: determination of the splice sites in ndhA and ndhB pre mRNAs. Mol. Gen. Genet. 210:385–393.

    Article  PubMed  CAS  Google Scholar 

  • McFadden, G.I. 1990. Evidence that cryptomonad chloroplasts evolved from photosynthetic eukaryotic endosymbionts. J. Cell Sci. 95:303–308.

    CAS  Google Scholar 

  • Mereschkowsky, C. 1905. Über Natur and Ursprung der Chromatophoren im Pflanzenreiche. Biol. Centralb. 25:593–604.

    Google Scholar 

  • Mereschkowsky, C. 1910. Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen. Biol. Centralb. 30:278–303, 321–347, 353–367.

    Google Scholar 

  • Michalowski, C.B., B. Pfanzagl, W. Löffelhardt, and H.J. Bohnert. 1990. The cyanelle S10 spc ribosomal protein gene operon from Cyanophora paradoxa. Mol. Gen. Genet. 224:222–231.

    Article  PubMed  CAS  Google Scholar 

  • Mignot, J.P. and E. Brugerolle. 1975. Etude ultrastructurale du flagellé phagotrophe Colponema loxodes Stein. Protistologica 11:429–444.

    Google Scholar 

  • Moestrup, Ø. 1978. On the phylogenetic validity of the flagellar apparatus in green algae and other chlorophyll a and b containing plants. BioSystems 10:117–144.

    Article  PubMed  CAS  Google Scholar 

  • Neumann-Spallart, C., J. Jakowitsch, M. Kraus, M. Brandtner, H.J. Bohnert, and W. Löffelhardt. 1991. rps10, unreported for plastid DNAs, is located on the cyanelle genome of Cyanophora paradoxa and is cotranscribed with the str operon genes. Curr. Genet. 19:313–315.

    Article  PubMed  CAS  Google Scholar 

  • Oakley, B.R. and F.J.R. Taylor. 1978. Evidence for a new type of endosymbiotic organization in a population of the ciliate Mesodinium rubrum from British Columbia. BioSystems 10:361–369.

    Article  PubMed  CAS  Google Scholar 

  • Osafune, T., J.A. Schiff, and G. Hase. 1990. Immunolocalization of LHCPII apoprotein in the Golgi of Euglena. p. 735–738. In: Current Research in Photosynthesis,Vol. III, M. Baltscheffsky (ed.). Kluwer, Dordrecht.

    Google Scholar 

  • Pascher, A. 1929. Über die Natur der blaugrünen Chromatophoren des Rhizopoden Paulinella chromatophora. Zool. Anz. 81:189–194.

    Google Scholar 

  • Perasso, R., A. Baroin, L.H. Qu, J.P. Bachellerie, and A. Adoutte. 1989. Origin of the algae. Nature 339:142–144.

    Article  PubMed  CAS  Google Scholar 

  • Pichersky, E., J.M. Logsdon, J.M. McGrath, and R.A. Stasys. 1991. Fragments of plastid DNA in the nuclear genome of tomato: prevalence, chromosomal location, and possible mechanism of integration. Mol. Gen. Genet. 225:453–458.

    Article  PubMed  CAS  Google Scholar 

  • Ragan, M.A. 1989. Biochemical pathways and the phylogeny of the eukaryotes. p. 145–160. In: The Hierarchy of Life, B. Fernholm, K. Bremer, and H. Jörnvall (eds.). Elsevier.

    Google Scholar 

  • Raven, P.H. 1970. A multiple origin for plastids and mitochondria. Science 169:641–646.

    Article  PubMed  CAS  Google Scholar 

  • Remillard, S.P., E.Y. Lai, Y.Y. Levy, C. Fulton. 1990. Differential expression of a calcineurin B gene during Naegleria differentiation. J. Cell Biol. 111:355a.

    Google Scholar 

  • Rikin, A. and S.D. Schwartzbach. 1988. Extremely large and slowly processed precursors to the Euglena light-harvesting chlorophyll a/b binding proteins of photosystem II. Proc. Natl. Acad. Sci. USA 85:5117–5121.

    Article  PubMed  CAS  Google Scholar 

  • Ris, H. 1961. Ultrastructure and molecular organization of genetic systems. Can. J. Genet. Cytol. 3:95–120.

    PubMed  CAS  Google Scholar 

  • Ris, H. and W. Plant. 1962. Ultrastructure of DNA-containing areas in the chloroplast of Chlamydomonas. J. Cell Biol. 13:383–391.

    Article  PubMed  CAS  Google Scholar 

  • Schenk, H.E.A., K. Poralla, T. Härtner, R. Deimel, and D. Thiel. 1985. Lipids in Cyanophora paradoxa I. Unusual fatty acid patterns of Cyanocyta korschikoffiana. Int. J. Endocyt. Cell Res. 2:233–238.

    Google Scholar 

  • Schnepf, E. 1964. Zur Feinstruktur von Geosiphon pyriforme: Ein Versuch zur Deutung cytoplasmatischer Membranen und Kompartimente. Archiv. für Mikrobiologie 49:112–131.

    Article  Google Scholar 

  • Schnepf, E. 1969. Leucoplasten bei Nitschia alba. Oesterr. Bot. 116:65–69.

    Article  Google Scholar 

  • Schnepf, E. and G. Deichgräber. 1984. Myzocytosis, a kind of endocytosis with implications to compartmentation in endosymbiosis. Observations in Paulsenella (Dinophyta). Naturwiss. 71:218–219.

    Article  Google Scholar 

  • Schnepf, E. and M. Elbrächter. 1988. Cryptophycean-like double-membrane bound chloroplast in the dinoflagellate, Dinophysis Ehrenb.: evolutionary, phylogenetic and toxicological implications. Bot. Mar. 101:196–203.

    Google Scholar 

  • Shivji, M.S. 1991. Organization of the chloroplast genome in the red alga Porphyra yezoensis. Curr. Genet. 19:49–54.

    Article  CAS  Google Scholar 

  • Siemeister, G., C. Buchholz, and W. Hachtel. 1990. Genes for the plastid elongation factor Tu and ribosomal protein S7 and six tRNA genes on the 73 kb DNA from Astasia longa that resembles the chloroplast DNA of Euglena. Mol. Gen. Genet. 220:425–432.

    Article  PubMed  CAS  Google Scholar 

  • Stanier, R.Y. 1970. Some aspects of the biology of cells and their possible evolutionary significance. p. 1–38. In:Organization and Control in Prokaryotic Cells. Soc. Gen. Microbiol. Symp. 20, H.P. Charles and B.C.J.G. Knight (eds.). Cambridge University Press.

    Google Scholar 

  • Stewart, K.D. and K.R. Mattox. 1975. Comparative cytology, evolution, and classification of the green algae with some consideration on the origin of other organisms with chlorophylls a and b. Bot. Rev. 41:104–135.

    Article  Google Scholar 

  • Stevenson, J.K., R.G. Drager, D.W. Coppertino, D.A. Christopher, K.P. Jenkins, G. Yepiz-Plascencia, and R.B. Hallick. 1991. Intercistronic group III introns in polycistronic ribosomal protein operons of chloroplasts. Mol. Gen. Genet. 222:183–192.

    Google Scholar 

  • Taylor, F.J.R. 1978. Problems in the development of an explicit hypothetical phylogeny of the lower eukaryotes. BioSysters 10:67–89.

    Article  CAS  Google Scholar 

  • Tessier, L.-H., M. Keller, R.L. Chan, R. Fournier, J.H. Weil, and P. Imbault. 1991. Short leader sequences may be transferred from small RNAs to pre-mature mRNAs by trans-splicing in Euglena. EMBO J. 10:2621–2625.

    PubMed  CAS  Google Scholar 

  • Thomsen, H.A. and K. Oates. 1978. Balaniger balticus gen. et sp. nov. (Prymnesiophyceae) from Danish coastal waters. J. Mar. BioL Assoc. UK 58:773–779.

    Article  Google Scholar 

  • Tomas, R.N. and E.R. Cox. 1973. Observations on the symbiosis of Peridinium balticum and its intracellular alga. I. Ultrastructure. J. Phycol. 9:304–323.

    Google Scholar 

  • Triemer, R.E. and M.A. Farmer. 1991. An ultrastructural comparison of the mitotic apparatus, feeding apparatus, flagellar apparatus and cytoskeleton in euglenoids and kinetoplastids. Protoplasma 164:91–104.

    Article  Google Scholar 

  • Turner, S., T. Burger-Wiersma, S.J. Giovannoni, C.R. Mur, and N.R. Pace. 1989. The relationship of a prochlorophyte Prochlorothrix hollandica to green chloroplasts. Nature 337:380–382.

    Article  PubMed  CAS  Google Scholar 

  • Urbach, E., D.L. Robertson, and S.W. Chisholm. 1992. Multiple evolutionary origins of prochlorophytes within the cyanobacterial radiation. Nature 355:267–270.

    Article  PubMed  CAS  Google Scholar 

  • van Valen, L.M. 1986. Proalgae and the significance of adaptive facies. Evol. Theory 8:29.

    Google Scholar 

  • Whatley, J.M., P. John, and F.R. Whatley. 1979. From extracellular to intracellular: the establishment of mitochondria and chloroplasts. Proc. Roy. Soc. Lond. B. 204:165–187.

    Article  CAS  Google Scholar 

  • Wilcox, L.W. 1989. Multilayered structures in two dinoflagellates, Katodinium campylops and Woloszynskia paschal. J. Phycol. 25:785–789.

    Article  Google Scholar 

  • Wilcox, L.W. and G.J. Wedermeyer. 1984. Gymnodinium acidotum Nygaard (Pyrrophyta), a dinoflagellate with an endosymbiotic cryptomonad. J. Phycol. 20:236–242.

    Article  Google Scholar 

  • Wilcox, L.W. and G.J. Wedermeyer. 1985. Dinoflagellates with chloroplast derived from an endosymbiotic eukaryote. Science 227:192–194.

    Article  PubMed  CAS  Google Scholar 

  • Wilhelm, C. 1987. The existence of chlorophyll c in the Chl b-containing, light-harvesting complex of the green alga Mantoniella squamata (Prasinophyceae). Bot. Acta 101:7–10.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Canadian Institute for Advanced Research Evolutionary Biology Program Department of Botany, The University of British Columbia, #3529-6270 University Blvd, Vancouver, B.C., V6T 1Z4, Canada

    Tom Cavalier-Smith

Authors
  1. Tom Cavalier-Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Marine Biology Research Division, 0202 Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA, 92093-0202, USA

    Ralph A. Lewin

Rights and permissions

Reprints and permissions

Copyright information

© 1992 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Cavalier-Smith, T. (1992). The Origin, Losses and Gains of Chloroplasts. In: Lewin, R.A. (eds) Origins of Plastids. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-2818-0_15

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-2818-0_15

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-6218-0

  • Online ISBN: 978-1-4615-2818-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation