Summary
The euglenoids and kinetoplastids form a diverse assemblage of organisms which show no obvious phylogenetic relationship with other flagellates. An ultrastructural examination and comparison of the flagellar apparatus, the feeding apparatus, and mitotic nucleus indicate a number of shared morphological features which support a common ancestry for the two groups. Of particular interest is the euglenoid,Petalomonas cantuscygni, which shares many of the ultrastructural features common to both groups. Based on the data presented, we hypothesize that a euglenoid with features similar to those now present inP. cantuscygni was ancestral to both the euglenoid and kinetoplastid lines.
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Abbreviations
- MTR:
-
complex of reinforcing microtubules
References
Balaban N, Waithaka HK, Njogu AR, Goldman R (1989) Isolation of a subpellicular microtubule protein fromTrypanosoma brucei that mediates crosslinking of microtubules. Cell Motil Cytoskeleton 14: 393–400
Bianchi L, Rondanelli EG, Carosi G, Gerna G (1969) Endonuclear mitotic spindle in the leptomonad ofLeishmania tropica. J Parasitol 55: 1091–1092
Bouck GB (1971) The structure, origin, isolation and composition of the tubular mastigonemes of theOchromonas flagellum. J Cell Biol 50: 362–384
Bouck GB (1972) Architecture and assembly of mastigonemes. Adv Cell Mol Biol 2: 237–271
—, Rogalski A, Valaitis A (1978) Surface organization and composition ofEuglena II. Flagellar mastigonemes. J Cell Biol 77: 805–826
Bramblett GT Kambadur R, Flavin M (1989) Immunocytochemical studies with antibodies to three proteins prominent in the isolated microtubule cytoskeleton of a trypanosomatid. Cell Motil Cytoskeleton 13: 145–157
Brooker BE (1971) Fine structure ofBodo saltans andBodo caudautus. (Zoomastigophora: Protozoa) and their affinities with the Trypanosomatidae. Bull Br Mus Nat Hist 22: 89–102
Brugerolle G (1973) Étude ultrastructurale du trophozoite et du kyste chez le genreChilomastix Alexieff 1910 (Zoomastigophorea, Retortomonadida, Grassé 1952). J Protozool 20: 574–585
— (1977) Ultrastructure du genreRetorlomonas Grassi 1879 (Zoomastigophorea, Retortomonadida, Wenrich 1932). Protistologica 8: 233–240
—, Joyon L (1975) Étude cytologique ultrastructurale des genresProteromonas etKarotomorpha (Zoomastigophorea, Proteromonadida, Grassé 1952). Protistologica 11: 531–546
—, Lom J, Nohynkova E, Joyon L (1979) Comparison et des structures cellulaires chez plusiers espèces de Bodonides et Cryptobiides appartenantaux genresBodo, Cryptobia etTrypanoplasma (Kinetoplastida Mastigorphora). Protistologica 15: 197–221
Burzell LA (1973) Observations on the proboscis-cytopharynx complex and flagella ofRhynchomonas metabolita Pshenin, 1964 (Zoomastigophorea: Bodonidae). J Protozool 20: 385–393
— (1975) Fine structureof Bodo curvifilus Griessman (Kinetoplastida: Bodonidae). J Protozool 22: 35–39
Cachon J, Cachon M, Cosson M-P, Cosson J (1988) The paraflagellar rod: a structure in search of a function. Biol Cell 63: 169–181
Cavalier-Smith T (1981) Eukaryote kingdoms: seven or nine? Bio Systems 14: 461–481
Chaley N, Lord A, LaFontaine G (1977) A light and electron microscopic study of nuclear structure throughout the cell cycle in the euglenoidAstasia longa. J Cell Sci 27: 23–45
Corliss JO (1984) The kingdom Protista and its 45 phyla. BioSystems 17: 87–126
Croft SL (1979) Ultrastructural study of the nucleus of Leishmania hertigi. Protistologica 15: 103–110
Cuhna NL, De Souza W, Hasson-Voloch A (1984) Isolation of the flagellum and characterization of the paraxial structure ofHerpetomonas megaseliae. J Submicrosc Cytol 16: 705–713
De Souza W, Meyer H (1974) On the fine structure of the nucleus inTrypanosoma cruzi in tissue culture forms. Spindle fibers in the dividing nucleus. J Protozool 21: 48–52
—, Souto-Padron T (1980) The paraxial structure of the flagellum. Trypanosomatidae. J Parasitol 66: 229–235
—, Rossi MA, Kitajima EW, Santos R, Roitman I (1976) An electron microscopic study ofHerpetomonas sp. (Leishmaniapessoai). Can J Microbiol 22: 197–203
Dodge JD (1975) The fine structure ofTrachelomonas (Euglenophyceae). Arch Protistenk 117: 65–77
Dougherty EC (1955) Comparative evolution and the origin of sexuality. Syst Zool 4: 145–169
Eyden BP (1977) Morphology and ultrastructure ofBodo designis Skuja 1948. Protistologica 13: 169–179
Farina M, Attias M, Souto-Padron T, De Souza W (1986) Further studies on the organization of the paraxial rod of trypanosomatids. J Protozool 33: 552–557
Farmer MA (1988) A re-evaluation of the taxonomy of the Euglenophyceae based on ultrastructural characteristics. PhD thesis, Rutgers University, Piscataway, NJ
—, Triemer RE (1988 a) Flagellar systems in the euglenoid flagellates. BioSystems 21: 283–291
— — (1988 b) A redescription of the genusPloeotia Duj. (Euglenophyceae). Taxon 37: 319–325
Foissner W, Blatterer H, Foissner I (1988) The Hemimastigophora (Hemimastix amphikineta nov. gen., nov. spec.), a new protistan phylum from Gondwanian soils. Eur J Protistol 23: 361–383
Freymuller E, Camargo EP (1981) Ultrastructural differences between species of trypanosomatids with and without endosymbionts. J Protozool 28: 175–182
Fritsch FE (1935) Structure and reproduction of the algae, vol 1. Cambridge University Press, London
Gallo J-M, Schrevel J (1985) Homologies between paraflagellar rod proteins from trypanosomes and euglenoids revealed by a monoclonal antibody. Eur J Cell Biol 36: 163–168
Gillott MA, Triemer RE (1978) Ultrastructure of cell division inEuglena. J Cell Sci 31: 25–36
Heimann K, Reize IB, Melkonian M (1989a) The flagellar developmental cycle in algae: flagellar transformation inCyanophora paradoxa (Glaucocystophyceae). Protoplasma 148: 106–110
—, Benting J, Timmermann S, Melkonian M (1989 b) The flagellar developmental cycle in algae: two types of flagellar development in uniflagellated algae. Protoplasma 153: 14–23
Heywood P, Weinmann D (1978) Mitosis in the hemoflagellateTrypanosoma cyclops. J Protozool 25: 287–292
Hibberd DJ, Leedale GF (1970) Eustigmatophyceae —a new algal class with unique organization of the motile cell. Nature 225: 759–760
— — (1971) A new algal class —the Eustigmatophyceae. Taxon 20: 523–525
— — (1972) Observations on the cytology and ultrastructure of the new algal class, Eustigmatophyceae. Ann Bot 36: 49–71
Hitchen ET (1974) The fine structure of the colonial kinetoplastid flagellateCephalothamnion cyclopum Stein. J Protozool 21: 221–231
Hollande A (1952) Classe des eugleniens (Euglenoidina Butschli, 1884). In: Grasse PP (ed) Traite de zoologie, vol 1, fasc 1. Mason, Paris, pp 238–284
Honigberg BM (1963) A contribution to systematics of the nonpigmented flagellates. In: Ludvik J, Lom J, Vavra J (eds) Progress in protozoology. Academic Press, New York, pp 68–69
—, Balamuth M, Bovee EC, Corliss JO, Godjics M, Hall RP, Kudo RR, Levine ND, Loeblich AR Jr, Weiser J, Weinrich DH (1964) A revised classification of the phylum Protozoa. J Protozool 11: 7–20
Hyams JS (1982) TheEuglena paraflagellar rod: structure, relationship to other flagellar components and preliminary biochemical characterization. J Cell Sci 55: 199–210
Inoki S, Ozeki Y (1969) Electron microscopic observations on division of kinetoplasts inTrypanosoma gambiense. Biken J 12: 31–41
Kivic PA, Walne PL (1984) An evaluation of a possible phylogenetic relationship between the Euglenophyta and Kinetoplastida. Orig Life 13: 269–288
Klebs G (1883) Über die Organisation einiger Flagellaten-Gruppen und ihre Beziehungen zu Algen und Infusorien. Unters Inst Tübingen 1: 233–362
Kugrens P, Rosowski JR (1972) Ultrastructure of mitosis inColacium. J Phycol 8: 9 a
Leedale GF (1967) Euglenoid flagellates. Prentice Hall, Englewood Cliffs, NJ
— (1968) The nucleus inEuglena. In: Buetow DE (ed) The biology ofEuglena. Academic Press, New York, pp 185–272
— (1970) Observations on the mitochondrial reticulum in livingEuglena gracilis. Cytobiologie 1: 195–202
— (1978) Phylogenetic criteria in euglenoid flagellates. BioSystems 10: 183–187
— (1982) Ultrastructure. In: Buetow DE (ed) The biology ofEuglena, vol 3. Academic Press, New York, pp 1–27
Margulis L, Corliss JO, Melkonian MM, Chapman DJ (eds) (1989) Handbook of Protoctista. Jones and Bartlett, Boston
Melkonian M, Reize IB, Preisig HR (1987) Maturation of a flagellum/basal body requires more than one cell cycle in algal flagellates: studies onNephroselmis olivacea (Prasinophyceae). In: Wiessner W, Robinson DG, Starr RCJ (eds) Algal development. Molecular and cellular aspects. Springer Berlin Heidelberg New York Tokyo, pp 102–113
Mignot J-P (1964) Observations complementaires sur la structure des flagelles d'Entosiphon sulcatum (Duj.) Stein, flagelle euglenien. Acad Sci Paris 258: 3360–3363
— (1966) Structure et ultrastructure de quelques euglenomonadines. Protistologica 2: 51–117
—, Brugerolle G, Bricheux G (1987) Intercalary strip development and dividing cell morphogenesis in the euglenidCyclidiopsis acus. Protoplasma 139: 51–65
Moestrup Ø (1982) Flagellar structure in algae: a review, with new observations particularly on the Chrysophyceae, Phaeophyceae (Fucophyceae), Euglenophyceae, andReckertia. Phycologia 21: 427–528
—, Hori T (1989) Ultrastructure of the flagellar apparatus inPyramimonas octopus (Prasinophyceae). II. Flagellar roots, connecting fibers, and numbering of individual flagella in green algae. Protoplasma 148: 41–56
Mylnikov AP (1986) Ultrastructure of a colorless flagellatePhyllomitus apiculatus Skuja 1948 (Kinetoplastida). Arch Protistenk 132: 1–10
Nisbet B (1974) An ultrastructural study of the feeding apparatus inPeranema trichophorum. J Protozool 21: 39–48
Nohynkova E (1984) A new pathogenicCryptobia from freshwater fishes: a light and electron microscopic study. Protistologica 20: 181–195
Owens K, Farmer MA, Triemer RE (1988) The flagellar apparatus and reservoir/cytoskeleton ofCryptoglena pigra (Euglenophyceae). J Phycol 24: 520–528
Patterson WB, Woo PTK (1984) Ultrastructural studies on mitosis inTrypanosoma danilewskyi (Mastigophora: Zoomastigophorea). Can J Bot 62: 1167–1171
Paulin JJ (1969) Ultrastructural observations on the kinetosome cycle ofCrithidia fasciculata and its significance to other members of the order (Kinetoplastida). Trans Am Microsc Soc 88: 400–410
Pickett-Heaps JD, Weik KL (1977) Cell division inEuglena andPhacus I. Mitosis. In: Rost TL, Gifford EM Jr (eds) Mechanisms and control of cell division. Academic Press, New York, pp 308–336
Porter D (1973)Isonema papillatum sp. n., a new colorless marine flagellate: a light and electron microscopic study. J Protozool 20: 351–356
Preston TM (1969) The form and function of the cytostome-cytopharynx of the culture forms of the elasmobranch haemoflagellateTrypanosoma raiae Laveran & Mesnil. J Protozool 16: 320–333
Raikov IB (1982) The protozoan nucleus. Springer, Wien New York [Alfert M et al (eds) Cell biology monographs, vol 9]
Russell DG, Newsam RJ, Palmer GCN, Gull K (1983) Structural and biochemical characterization of the paraflagellar rod ofCrithidia fasciculata. Eur J Cell Biol 30: 137–143
Schlaeppi K, Deflorin J, Seebeck T (1989) The major component of the paraflagellar rod ofTrypanosoma brucei is a helical protein that is encoded by two identical, tandemly linked genes. J Cell Biol 109: 1695–1709
Schuster FL, Goldstein S, Hershenov B (1968) Ultrastructure of a flagellate,Isonema nigricans nov. gen. nov. sp. from a polluted marine habitat. Protistologica 4: 141–149
Senn G (1900) Flagellata. In: Engler A, Prantl K (eds) Die natürlichen Planzenfamilien, vol 1. W Engelmann, Leipzig, pp 93–188
Sherwin T, Gull K (1989) The cell division cycle ofTrypanosoma brucei brucei: timing of event markers and cytoskeletal modulations. Philos Trans R Soc Lond [Biol] 323: 573–588
Skarlato SO (1987) Fine structural pecularities of the nucleus of the parasitic flagellateTrypanosoma borelli. Rep Acad Sci USSR 293: 220–221
Sogin ML, Elwood HJ, Gunderson JH (1986) Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proc Natl Acad Sci USA 83: 1383–1387
Solari AJ (1980 a) Function of the dense plaques during mitosis inTrypanosoma cruzi. Exp Cell Res 127: 457–460
— (1980 b) The 3-dimensional fine structure of the mitotic spindle inTrypanosoma cruzi. Chromosoma 78: 239–255
— (1983) The ultrastructure of mitotic nuclei ofBlastocrithidia triatomae. Z Parasitenk 69: 3–15
Sommer JR, Blum JJ (1965) Cell division inAstasia longa. Exp Cell Res 39: 504–527
Souto-Padron T, Gon Calves de Lima VMQ, Roitman I, De Souza W (1980) An electron microscopic and cytochemical study ofLeptomonas samueli. Z Parasitenk 62: 127–143
Steinert M, Novikoff AB (1960) The existence of a cytostome and the occurrence of pinocytosis in the trypanosome,Trypanosoma mega. J Biophys Biochem Cytol 8: 563–569
Surek B, Melkonian M (1986) A cryptic cytostome inEuglena. Protoplasma 133: 39–49
Swale EMF (1973) A study of the colourless flagellateRhynchonomonas nasuta (Stokes) Klebs. Biol J Linn Soc 5: 255–264
Taylor FJR (1976) Flagellate phytogeny: a study in conflicts. J Protozool 23: 28–40
— (1980) The stimulation of cell research by endosymbiotic hypotheses for the origin of the eukaryotes. In: Schwemmer W, Schenk HEA (eds) Endocytobiology. W de Gruyter, Berlin, pp 917–947
Triemer RE (1985) Ultrastructural features of mitosis inAnisonema sp. (Euglenida). J Protozool 32: 683–690
— (1986) Light and electron microscopic description of a colorless euglenoid,Serpenomonas costata n. g., n. sp. J Protozool 33: 412–415
— (1988) Ultrastructure of mitosis inEntosiphon sulcatum (Euglenida). J Protozool 35: 53–59
—, Farmer MA (1988)Petalomonas cantuscygni, a possible evolutionary link between the euglenoids and the kinetoplastids. J Phycol 24: 22 a
Triemer RE, Fritz L (1986) Structure and operation of the feeding apparatus in a colorless euglenoid,Entosiphon sulcatum. J Protozool 34: 154–162
— — (1988) Ultrastructural features of mitosis inPloeotia costata (Heteronematales, Euglenophyta). J Phycol 24: 514–519
—, Ott DW (1990) Ultrastructure ofDiplonema ambulator Larsen & Patterson (Euglenozoa) and its relationship toIsonema. Eur J Protozool 25: 316–320
—, Fritz L, Herman R (1986) Fine structure of mitosis inLeishmania adlerii. Protoplasma 134: 154–162
Vickerman K (1977) DNA throughout the single mitochondrion of a kinetoplastid flagellate: observations on the ultrastructure ofCryptobia vaginalis (Hesse 1910). J Protozool 24: 221–233
— (1989) Phylum Zoomastigina class Kinetoplastida. In: Margulis L, Corliss JO, Melkonian M, Chapman DJ (eds) Handbook of Protoctista. Jones and Barlett, Boston, pp 215–238
—, Preston TM (1970) Spindle microtubules in the dividing nuclei of trypanosomes. J Cell Sci 6: 365–383
— — (1976) Comparativecell biology of the kinetoplastid flagellates. In: Lumsden HR, Evans DA (eds) Biology of the Kinetoplastida. Academic Press, London, pp 35–130
Willey RL, Wibel RG (1985 a) The reservoir cytoskeleton and a possible cytostomal homologue inColacium (Euglenophyceae). J Phycol 21: 570–577
— — (1985 b) A cytostome/cytopharynx in green euglenoid flagellates (Euglenales) and its phylogenetic implications. BioSystems 18: 369–367
— — (1987) Flagellar roots and the reservoir cytoskeleton ofColacium libellae (Euglenophyceae). J Phycol 23: 283–288
—, Walne PL, Kivic P (1988) Phagotrophy and the origins of the euglenoid flagellates. CRC Crit Rev Plant Sci 7: 303–340
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Triemer, R.E., Farmer, M.A. An ultrastructural comparison of the mitotic apparatus, feeding apparatus, flagellar apparatus and cytoskeleton in euglenoids and kinetoplastids. Protoplasma 164, 91–104 (1991). https://doi.org/10.1007/BF01320817
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DOI: https://doi.org/10.1007/BF01320817