Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-20T00:54:01.081Z Has data issue: false hasContentIssue false

Sexual processes in the kinetoplastida

Published online by Cambridge University Press:  06 April 2009

A. Tait
Affiliation:
Department of Genetics, University of Edinburgh, West Mains Road, Edinburgh

Summary

The commonly held view that the kinetoplastida, and in particular trypanosomes, are asexual is largely derived from the principle that an organism is asexual until proved sexual. If the basis for this view is examined in detail, it largely arises from the lack of morphologically distinguishable gametes, the difficulties encountered in visualizing chromosomes and a few experiments, using drug-resistant stocks, in which no recombination between stocks could be demonstrated. While it is clear that these organisms are able to reproduce asexually, the existence of a sexual cycle was, until recently, an entirely open question. The early work strongly suggests that any sexual process (in the species examined extensively at the morphological level) does not involve classical well-differentiated gametes and so must involve fusion of morphologically very similar cells. These findings taken together with the inability to visualize chromosomes and thereby identify meiosis, mean that classical methods are unable to detect any sexual process even if it did occur. This review examines the evidence provided by the experimental approaches which have been applied recently to the question of kinetoplastid sexuality. These approaches include isoenzyme studies and the analysis of possible genetic exchange by the use of selective markers (e.g. drug resistance). The results which these techniques have produced make it clear that the kinetoplastid protozoans cannot be regarded as a totally asexual group of organisms.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1983

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aleman, C. (1969). Fine. structure of cultured L. braziliensis. Experimental Parasitology 24, 259264.Google Scholar
Al-Taqi, M. & Evans, D. A. (1978). Characterisatio of Leishmania spp from Kuwait by iso-enzyme electrophoresis. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 56–5.CrossRefGoogle Scholar
Aljeboom, T. I. & Evans, D. A. (1980 a). Leishmania spp in Iraq. Electrophoretic iso-enzyme patterns. I. Visceral Leishmaniasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 169–77.CrossRefGoogle Scholar
Aljeboori, T. I. & Evans, D. A. (1980 b).Leishmania spp in Iraq. Electrophoretic iso-enzyme patterns. II. Cutaneous Leishmaniasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 178–84.CrossRefGoogle Scholar
Amrein, Y. U. (1957). Evidenc against sexuality in Trypanosoma gambiense. Journal of Protozoology 4, 67–8.CrossRefGoogle Scholar
Amrein, Y. U. (1965). Genetic transfer in trypanosomes. I. Syngamy in T. cruzi. Experimental Parasitology 17, 261–3.Google Scholar
Amrein, Y. U. & Fulton, J. D. (1959). Attempt to transfer drug resistance of trypanosomes in vivo. Journal of Protozoology 6, 120–2.CrossRefGoogle Scholar
Bagstee, I. A. & Parr, C. W. (1973). Trypanosome identification by electrophoresis of soluble enzymes. Nature, London 244, 364–6.CrossRefGoogle Scholar
Baker, J. R. (1978). Discussion group on protozoology. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 109–12.Google Scholar
Baker, J. R. & Price, J. (1973). Growth in vitro of T. cruzi as amastigotes at temperatures below 37 °C. International Journal for Parasitology 3, 549–51.CrossRefGoogle Scholar
Baker, J. R., Miles, M. A., Godfrey, D. G. & Barrett, T. V. (1978). Biochemical characterisation of some species of trypanosomes from bats (Microchiroptera). American Journal of Tropical Medicine and Hygiene 27, 483–95.Google Scholar
Belnat, P., Paoletti, J. & Riou, G. (1981). Subunit organisation of chromatin from T. cruzi sensitive and resistant to Ethidium bromide. Molecular and Biochemical Parasitology 2, 167–76.CrossRefGoogle Scholar
Borst, P. & Cross, G. A. M. (1982). Molecular basis for trypanosome antigenic variation. Cell, 29, 291303.CrossRefGoogle ScholarPubMed
Borst, P., Fase-Fowler, F., Frasch, A. C. C., Hoeijmakers, J. H. J. & Weijers, P. J. (1980). Characterisation of DNA from Trypanosoma brucei and related trypanosomes by restriction endonuclease digestion. Molecular and Biochemical Parasitology 1, 221–46.Google Scholar
Borst, P. & Hoeijmakers, J. H. J. (1979). Kinetoplast DNA. Plasmid 2, 2040.Google Scholar
Borst, P., Van der Ploeg, M., Van Hoek, J. F. M., Tas, J. & James, J. (1982). On the DNA content and ploidy of trypanosomes. Molecular and Biochemical Parasitology 6, 1323.CrossRefGoogle ScholarPubMed
Bray, R. S. (1974). Leishmania. Annual Review of Microbiology 28, 189218.CrossRefGoogle ScholarPubMed
Brenner, Z. (1972). A new aspect of T. cruzi life cycle in the invertebrate host. Journal of Protozoology 19, 23–7.CrossRefGoogle Scholar
Byers, B. & Goetsch, L. (1975). Electron microscopic observations on the meiotic karyotype of diploid and tetraploid S. cerevisiae. Proceedings of the National Academy of Sciences 72, 5056–60.CrossRefGoogle Scholar
Carter, R. (1973). Enzyme variation in P. berghei and P. vinckei. Parasitology 66, 297307.CrossRefGoogle Scholar
Castro, C., Craig, S. P. & Castaneda, M. (1981). Genome organisation and ploidy number in T. cruzi. Molecular and Biochemical Parasitology 4, 273–82.CrossRefGoogle Scholar
Chagas, C. (1909). Ueber eine neue Trypanosomiasis des Menschen. Studien über Morphologie und Entwicklungszyklus des Schizotrypanum cruzi n.gen., n.s.p., Erreger einer neuen Krankheit des Menschen. Memorias do Instituto Oswaldo Cruz 1, 159218.CrossRefGoogle Scholar
Chagas, C. (1927). Quelques aspects evolutifs du Trypanosoma cruzi dans l'insecte transmetteur. Comptes rendus des séances de la Societe de Biologie 97, 829–32.Google Scholar
Chance, M. L. (1979). The identification of Leishmania. In Problems in the Identification of Parasites and their Vectors (ed. Taylor, A. E. R. and Muller, R.), pp. 5574. Oxford: Blackwell Scientific Publications.Google Scholar
Chance, M. L., Schnur, L. F., Thomas, S. C. & Peters, W. (1978). The biochemical and serological taxonomy of Leishmania from the Aethiopian zoogeographical region of Africa. Annals of Tropical Medicine and Parasitology 72, 533–42.CrossRefGoogle ScholarPubMed
Deane, M. P. & Milder, R. (1966). A process of reproduction of T. conorhini different from binary or multiple fission. Journal of Protozoology 13, 553–9.Google Scholar
Deane, M. P. & Milder, R. (1972). Ultrastructure of the cyst like bodies of T. conorhini. Journal of Protozoology 19, 2842.Google Scholar
De Souza, W. & Meyer, H. (1974). On the fine structure of the nucleus of T. cruzi in tissue culture forms. Spindle fibres in the dividing nucleus. Journal of Protozoology 21, 4852.Google Scholar
Elkeles, G. (1944). Investigaciones sobre la evolucion de T. cruzi especialmente sobre la genesis de la forma trypanosomica. Boletin Academia de Cordoba 36, 330408.Google Scholar
Ellis, D. S. & Evans, D. A. (1977). Electron microscope studies of 'cyst like bodies' found in cultures of T.b. rhodesiense. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 385.Google Scholar
Ellestrand, N. C. & Levin, D. A. (1980). Recombinatio system and population structure in Oenothera. Evolution 34, 923–33.CrossRefGoogle Scholar
Fairbairn, H., Culwick, A. F. & Gee, F. L. (1946). A new approach to trypanosomiasis. Annals of Tropical Medicine and Parasitology 40, 421–52.CrossRefGoogle ScholarPubMed
Falconer, D. S. (1977). Introduction to Quantitative Genetics. London: Longman Ltd.Google Scholar
Ferguson, A. (1980). Biochemical Systematics and Evolution. Glasgow: Blackie.Google Scholar
Fiennes, R.N. (1945). A sexual reproduction cycle of T. congolense. Nature, London 156, 390–1.Google Scholar
Gardener, P. J., Chance, M. L. & Peters, W. (1974). Biochemical taxonomy of Leishmania. II. Electrophoretic variation of malate dehydrogenase. Annals of Tropical Medicine and Parasitology 68, 317–25.CrossRefGoogle ScholarPubMed
Garnham, P. C. C. (1966). Malaria Parasites and Other Haemosporidia. Oxford: Blackwell Scientific Publications.Google Scholar
Gibson, W. C., Parr, C. W., Swindlehurst, C. A. & Welch, S. G. (1978). A comparison of the iso-enzymes, soluble proteins, polypeptides and free amino acids from ten isolates of T. evansi. Comparative Biochemistry and Physiology 60B, 137–42.Google Scholar
Gibson, W. C., Marshall, T. F. de C. & Godfrey, D. G. (1980). Numerical analysis of enzyme polymorphism. A new approach to the epidemiology and taxonomy of trypanosomes of the sub-genus Trypanozoon. Advances in Parasitology 18, 175245.Google Scholar
Godfrey, D. G. (1979). The zymodemes of trypanosomes. Symposia of the British Society for Parasitology 17, 3153.Google Scholar
Godfrey, D. G. (1982). Biochemical characterisation in the taxonomy of parasitic protozoa. In Biochemical Characterisation of Leishmania, pp. 6372. UNDP/World Bank/WHO, Geneva.Google Scholar
Godfrey, D. G. & Kilgour, V. (1976). Enzyme electrophoresis in characterising the causative organisms of Gambian trypanosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 219–24.Google Scholar
Goncalves de Lima, V. M. Q., Roitman, I. & Kilgour, V. (1979). Five trypanosomatid species of insects distinguished by iso-enzymes. Journal of Protozoology 24, 648–52.CrossRefGoogle Scholar
Grell, K. G. (1967). Sexual reproduction in Protozoa. In Research in Protozoology, vol. 2, pp. 149213. Oxford: Pergamon Press.Google Scholar
Grell, K. G. (1973). Protozoology. Berlin: Springer-Verlag.Google Scholar
Hardy, G. H. (1908). Mendelian proportions in a mixed population. Science 28, 4950.CrossRefGoogle Scholar
Harris, H. (1969). Genes and isozymes. Proceedings of the Royal Society of London B 174, 131.Google Scholar
Harris, H. & Hopkinson, D. A. (1976). Handbook of Enzyme Electrophoresis in Human Genetics. Amsterdam: North Holland.Google Scholar
Hoare, C. A. (1972). The Trypanosomes of Mammals. Oxford: Blackwell Scientific Publications.Google Scholar
Hughes, D. E., Schneider, C. A. & Simpson, L. (1982 a). Flagellar adherence of C. fasculata cells in culture. Molecular and Biochemical Parasitology, Suppl. 109.Google Scholar
Hughes, D. E., Schneider, C. A. & Simpson, L. (1982 b). Isolation and characterization of drug resistant mutants of C. fasculata. Journal of Parasitology (in the Press).Google Scholar
Kilgour, V. & Godfrey, D. G. (1973). Species characteristic iso-enzymes of two amino transferases in trypanosomes. Nature, (New Biology) 244, 6970.Google Scholar
Kreutzer, R. D. & Christensen, H. A. (1980). Characterisation of Leishmania spp. by iso-enzyme electrophoresis. American Journal of Tropical Medicine and Hygiene 29, 199208.Google Scholar
Kreutzer, R. D. & Souza, O. E. (1981). Biochemical characterisation of Trypanosoma spp. by iso-enzyme electrophoresis. American Journal of Tropical Medicine and Hygiene 30, 308–17.Google Scholar
Lanar, D. E., Levy, L. S. & Manning, J. E. (1981). Complexity and content of the DNA and RNA in T. cruzi. Molecular and Biochemical Parasitology 3, 327–41.Google Scholar
Lewontin, R. C. (1974). The Genetic Basis of Evolutionary Change. New York: Columbia University Press.Google Scholar
Lush, I. E. (1966). The Biochemical Genetics of Vertebrates except Man. Amsterdam: North Holland.Google Scholar
Mehlitz, D., Zilmann, U., Scott, C. M. & Godfrey, D. G. (1982). Epidemiological studies on the animal reservoir of Gambiense sleeping sickness. Part III. Characterization of Trypanozoon stocks by iso-enzymes and sensitivity to human serum. Tropenmedizin und Parasitologie 33, 113–18.Google Scholar
Miles, M. A. (1979). Transmission cycles and heterogeneity of T. cruzi. In Biology of the Kinetoplastida, vol. 2, pp. 117196. London: Academic Press.Google Scholar
Miles, M. A., Lainson, R., Shaw, J. J., Povoa, M. & de Souza, A. A. (1981 a). Leishmaniasis in Brazil. XV. Biochemical distinction of Leishmania mexicana amazonensis, L. braziliensis braziliensis and L. braziliensis guyanensis - aetiological agents of cutaneous leishmaniasis in the Amazon basin of Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 524–9.Google Scholar
Miles, M. A., Lanham, S. M., de Souza, A. A. & Povoa, M. M. (1980). Further enzymic characters of T. cruzi and their evaluation for strain identification. Transactions of the Royal Society of Medical Hygiene 74, 221–37.CrossRefGoogle Scholar
Miles, M. A., Povoa, M. M., de Souza, A. A., Lainson, R. & Shaw, J. J. (1979). Some methods for the enzymic characterisation of Latin-American Leishmania with particular reference to L. mexicana amazonensis and sub-species of L. hertegi. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 243–52.Google Scholar
Miles, M. A., Povoa, M. M., de Souza, A. A., Lainson, R., Shaw, J. J. & Ketteridge, D. S. (1981 b). Chaga's disease in the Amazon basin. II. The distribution of T. cruzi zymodemes 1 and 3 in Para State, North Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 667–74.CrossRefGoogle ScholarPubMed
Miles, M. A., de Souza, A. A., Povoa, M. M., Shaw, J. J., Lainson, R. & Toye, P. J. (1978). Isozymic heterogeneity of T. cruzi in the first autochthonous patients with Chaga's diseases in Amazonian Brazil. Nature, London 272, 819–21.Google Scholar
Miles, M. A., Toye, P. J., Oswald, S. C. & Godfrey, D. G. (1977). The identification by iso-enzyme pattern of two distinct strain-groups of T. cruzi circulating independently in a rural area of Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 217–25.CrossRefGoogle Scholar
Milkman, R. (1973). Electrophoretic variation in E. coli from natural sources. Science 182, 1024–5.CrossRefGoogle Scholar
Milkman, R. (1976). Isoelectric focussing of MDH and 6-PGDH from E. coli of diverse natural origins. Biochemical Genetics 14, 517–22.CrossRefGoogle Scholar
Murray, A. K. (1982). Characterisation of stocks of T. vivax. I. Iso-enzyme studies. Annals of Tropical Medicine and Parasitology 76, 275–82.CrossRefGoogle Scholar
Noble, E. R. (1955). The morphology and life cycle of trypanosomes. Quarterly Review of Biology 30, 128.Google Scholar
Noble, E. R., McRary, W. L. & Beaver, E. T. (1953). Cell division in trypanosomes. Transactions of the American Microscopical Society 72, 236–48.CrossRefGoogle Scholar
Nyindo, M., Chimtawi, M. & Owor, J. (1981). Trypanosoma brucei: evidence suggesting existence of sexual forms of parasites cultured from the tsetse, Glossina morsitans morsitans. Insect. Sci. Appl. 1, 171–5.Google Scholar
Ormerod, W. E. (1979). Development of T. brucei in the mammalian host. In Biology of the Kinetoplastida, vol. 2, pp. 339384. London: Academic Press.Google Scholar
Pays, E., Lheureux, M. & Steinert, M. (1981). The expression linked copy of surface antigen gene in Trypanosoma is probably the one transcribed. Nature, London 292, 265–7.Google Scholar
Preer, J. R. Jr., (1968). Genetics of Protozoa. In Research in Protozoology vol. 3, pp. 133246. Oxford: Pergamon Press.Google Scholar
Rassam, M. B., Al-Mudhaffar, S. A. & Chance, M. L. (1979). Iso-enzyme characterisation of Leishmania species from Iraq. Annals of Tropical Medicine and Parasitology 73, 527–34.CrossRefGoogle Scholar
Ready, P. D. & Miles, M. A. (1979). Delimitation of T. cruzi zymodemes by numerical taxonomy. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 238–42.Google Scholar
Rubio, J., Rosado, Y. & Castaneda, M. (1980). Subunit structure of T. cruzi chromatin. Canadian Journal of Biochemistry 58, 1247–51.CrossRefGoogle ScholarPubMed
Schick, J. M. & Lamb, A. N. (1977). Asexual reproduction and genetic population structure in the colonizing sea anemone, H. Luciae. Biological Bulletin 153, 604–17.Google Scholar
Selander, R. K. & Kaufman, D. W. (1975). Genetic population structure and breeding systems. In Iso-enzyrnes, vol. 4, pp. 2748. London: Academic Press.Google Scholar
Sen Gupta, P. C., Bhattacharjee, B. & Ray, H. N. (1953). The cytology of Leishmania donnovani. Journal of the Indian Medical Association 22, 305–8.Google Scholar
Sen Gupta, P. C. & Ray, H. N. (1954). Observations on the nuclear structure of Leishmania donnovani Ross, 1903. Proceedings of the Zoological Society 7, 113–16.Google Scholar
Sinden, R. E. (1978). Cell biology. In Rodent Malaria (ed. Killick-Kendrick, R. and Peters, W.), pp. 85169. London: Academic Press.Google Scholar
Solari, A. J. (1980). The 3-dimensional fine structure of mitotic spindle in T. cruzi. Chromosoma 78, 239–55.Google Scholar
Tait, A. (1980). Evidence for diploidy and mating in trypanosomes. Nature, London 287, 536–8.Google Scholar
Tibayrenc, M., Breuiere, F., Echalar, L. & Cartier, Y. (1981 a). Donnees isoenzymatiques pour onze souches boliviennes de T. cruzi. Interpretation genetique et calcul de distances. Cahiers O.R.S.T.O.M. Ser. Biologie 19, 129–34.Google Scholar
Tibayrenc, M., Cariou, L. & Solignac, M. (1981 b). Interpretation genetique des zymogrammes de Flagelles des genues Trypanosoma et Leishmania. Comptes rendus, Academie des Sciences, Paris 292, 623–5.Google Scholar
Tibayrenc, M., Cariou, M., Solignac, M. & Cartier, Y. (1981 c). Arguments genetique coutre l'existence d'une sexualite actuelle chez T. cruzi. Implications taxinomiques. Comptes rendus, Academie des sciences, Paris 293, 207–9.Google Scholar
Toyé, P. J. (1974). Iso-enzyme variation in isolates of T. cruzi. Transactions of the Royal Society of Tropical Medicine and Hygiene 68, 147.Google Scholar
Vandeeplank, F. L. (1944). Identification of trypanosomes by chromosomes. Nature, London 154, 1920.Google Scholar
Vickermann, K. (1976). The diversity of the kinetoplastid flagellates. In Biology of the Kinetoplastida, vol. 1, pp. 134. London: Academic Press.Google Scholar
Vickermann, K. & Preston, T. M. (1970). Spindle microtubules in the dividing nuclei of trypanosomes. Journal of Cell Science 6, 365–84.CrossRefGoogle Scholar
Walliker, D., Carter, R. & Morgan, S. (1971). Genetic recombination in malaria. Nature, London 232, 561–2.Google Scholar
Walker, P. J. (1964). Reproduction and heredity in trypanosomes. International Review of Cytology 17, 5197.Google Scholar
Williams, R. O., Young, J. R. & Majiwa, P. A. O. (1982). Genomic environment of T. brucei VSG genes: presence of a minichromosome. Nature, London 299, 417–20.Google Scholar
Zimmerman, E. G., Kilpatrick, C. W. & Hart, B. J. (1978). The genetics of speciation in the rodent genus Peromyscus. Evolution 32, 565–79.Google Scholar