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Evidence that the mechanism of gene exchange in Trypanosoma brucei involves meiosis and syngamy

Published online by Cambridge University Press:  06 April 2009

C. M. R. Turner
Affiliation:
Department of Zoology, University of Glasgow, Glasgow G12 8QQ
J. Sternberg
Affiliation:
Department of Genetics, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT
N. Buchanan
Affiliation:
Wellcome Unit of Molecular Parasitology, Department of Veterinary Parasitology, University of Glasgow, Bearsden Road, Glasgow G61 1QH
E. Smith
Affiliation:
Department of Zoology, University of Glasgow, Glasgow G12 8QQ
G. Hide
Affiliation:
Wellcome Unit of Molecular Parasitology, Department of Veterinary Parasitology, University of Glasgow, Bearsden Road, Glasgow G61 1QH
A. Tait
Affiliation:
Wellcome Unit of Molecular Parasitology, Department of Veterinary Parasitology, University of Glasgow, Bearsden Road, Glasgow G61 1QH

Summary

All pairwise combinations of three cloned stocks of Trypanosoma brucei (STIB 247L, STIB 386AA and TREU 927/4) were co-transmitted through tsetse flies (Glossina morsitans) and screened for the production of hybrid trypanosomes. Clones of metacyclic and bloodstream trypanosomes from flies harbouring mature infections containing hybrid trypanosomes were established and screened for several isoenzyme and restriction fragment length polymorphisms. For each of the three combinations of parents, some progeny clones were observed to be of a phenotype and genotype indicating that genetic exchange had occurred during development of the trypanosomes in flies. These hybrid clones shared three salient features: (1) where the parents were homozygous variants the progeny were heterozygous, (2) where one of the parents was heterozygous, allelic segregation was observed and (3) the progeny clones were shown to be recombinant when two or more markers for which one of the parents was heterozygous were examined. These results are consistent with the progeny being an F1 in a diploid mendelian genetic system involving meiosis and syngamy. Our observations show that all possible combinations of the three stocks may undergo genetic exchange. A marker analysis of a series of clones each derived from single metacyclic trypanosomes showed that individual flies transmit a mixture of trypanosome genotypes corresponding to F1 progeny and to parental types, indicating that genetic exchange was a non-obligatory event in the life-cycle of the trypanosome. In addition, a preliminary analysis of the phenotype of procyclic stage trypanosomes derived from flies infected with two stocks, indicates that genetic exchange is unlikely to occur at this stage.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

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References

REFERENCES

Brun, R. & Schonenberger, M. (1979). Cultivation and in vitro cloning of procyclic culture forms of Trypanosoma brucei in semi-defined medium. Acta Tropica 36, 289–92.Google ScholarPubMed
Gibson, W. C. (1989). Analysis of a genetic cross between Trypanosoma brucei rhodesiense and T. b. brucei. Parasitology 99, 391402.CrossRefGoogle ScholarPubMed
Gibson, W. C., Marshall, T. F. D. C. & Godfrey, D. G. (1980). Numerical analysis of enzyme polymorphisms: new approach to the epidemiology and taxonomy of trypanosomes of the subgenus Trypanozoon. Advances in Parasitology 18, 175246.CrossRefGoogle Scholar
Gibson, W. C., Osinga, K. A., Michels, P. A. M. & Borst, P. (1985). Trypanosomes of the subgenus Trypanozoon are diploid for housekeeping genes. Molecular and Biochemical Parasitology 16, 231–42.CrossRefGoogle ScholarPubMed
Hajduk, S. L., Cameron, C. R., Barry, J. D. & Vickerman, K. (1981). Antigenic variation in cyclically transmitted Trypanosoma brucei. Variable antigen type composition of metacyclic trypanosome populations from the salivary glands of Glossina morsitans. Parasitology 83, 597607.Google Scholar
Jenni, L., Marti, S., Schweizer, J., Betschart, B., Le Page, R. W. F., Wells, J. M., Tait, A., Paindavoine, P., Pays, E. & Steinert, M. (1986). Hybrid formation between African trypanosomes during cyclical transmission. Nature, London 322, 173–5.CrossRefGoogle ScholarPubMed
Kaminsky, R., Beaudoin, E. & Cunningham, I. (1987). Studies on the development of metacyclic Trypanosoma brucei spp. cultivated at 27 °C with insect cell lines. Journal of Protozoology 34, 372–7.CrossRefGoogle Scholar
Kooy, R. F., Hirumi, H., Moloo, S. K., Nantulya, V. M., Dukes, P., Van DerLinden, P. M., Duijndam, W. A. L., Janse, C. J. K. & Overdulve, J. P. (1989). Evidence for diploidy in metacyclic forms of African trypanosomes. Proceedings of the National Academy of Sciences, USA 86, 5469–72.CrossRefGoogle ScholarPubMed
Lanham, S. W. & Godfrey, D. G. (1970). Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Experimental Parasitology 38, 521–34.CrossRefGoogle Scholar
Le Page, R. W. F., Wells, J. M., Prospero, T. D. & Sternberg, J. (1988). Genetic analysis of hybrid T. brucei. In Current Communications in Molecular Biology: Molecular Genetics of Parasitic Protozoa (ed. Turner, M. J. & Arnot, D.) Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.Google Scholar
Maudlin, I. & Dukes, P. (1985). Extrachromosomal inheritance of susceptibility of trypanosome infection in tsetse flies. 1. Selection of susceptible and refractory lines of Glossina morsitans morsitans. Annals of Tropical Medicine and Parasitology 79, 317–24.CrossRefGoogle ScholarPubMed
Maudlin, I. & Welburn, S. C. (1987). Lectin-mediated establishment of midgut infections of Trypanosoma congolense and Trypanosoma brucei in Glossina morsitans. Tropical Medicine and Parasitology 38, 167–70.Google ScholarPubMed
Paindavoine, P., Zambetti-Bosseler, F., Pays, E., Schweizer, J., Guyaux, M., Jenni, L. & Steinert, M. (1986). Trypanosome hybrids generated in tsetse flies by nuclear fusion. EMBO Journal 5, 3631–6.CrossRefGoogle ScholarPubMed
Schweizer, J., Tait, A. & Jenni, L. (1988). The timing and frequency of hybrid formation in African trypanosomes during cyclical transmission. Parasitology Research 75, 98101.CrossRefGoogle ScholarPubMed
Sternberg, J., Tait, A., Haley, S., Wells, J. M., Le Page, R. W. F., Schweizer, J. & Jenni, L. (1989). Gene exchange in African trypanosomes: characterisation of a new hybrid genotype. Molecular and Biochemical Parasitology 27, 191200.CrossRefGoogle Scholar
Sternberg, J., Turner, C. M. R., Wells, J. M., Randford-Cartwright, L. C., Le Page, R. W. F. & Tait, A. (1989). Gene exchange in African trypanosomes: frequency and allelic segregation. Molecular and Biochemical Parasitology 34, 269–80.CrossRefGoogle ScholarPubMed
Tait, A. (1980). Evidence for diplody and mating in trypanosomes. Nature, London 287, 536–8.CrossRefGoogle ScholarPubMed
Tait, A. (1983). Sexual processes in the Kinetoplastida. Parasitology 86, 2957.CrossRefGoogle ScholarPubMed
Tait, A., Babiker, E. A. & Le Ray, D. (1984). Enzyme variation in Trypanosoma brucei spp. I Evidence for the sub-speciation of Trypansoma brucei gambiense. Parasitology 89, 311–26.CrossRefGoogle Scholar
Tait, A., Turner, C. M. R., Le Page, R. W. F. & Wells, J. M. (1989). Genetic evidence that metacyclic forms of Trypanosoma brucei are diploid. Molecular and Biochemical Parasitology 73, 247–56.CrossRefGoogle Scholar
Tait, A. & Turner, C. M. R. (1990). Genetic exchange in Trypanosoma brucei. Parasitology Today 6, 70–5.CrossRefGoogle ScholarPubMed
Wellburn, S. C. & Maudlin, I. (1987). A simple in vitro method for infecting tsetse with trypanosomes. Annals of Tropical Medicine and Parasitology 81, 453–5.CrossRefGoogle Scholar
Wells, J. M., Prospero, T. D., Jenni, L. & Le Page, R. W. F. (1987). DNA contents and molecular karyotypes of hybrid Trypanosoma brucei. Molecular and Biochemical Parasitology 24, 103–16.CrossRefGoogle ScholarPubMed