Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-23T15:43:03.509Z Has data issue: false hasContentIssue false

Determination of nuclear DNA of five Eucoccidian parasites, Isospora (Toxoplasma) gondii, Sarcocystis cruzi, Eimeria tenella, E. acervulina and Plasmodium berghei, with special reference to gamontogenesis and meiosis in I. (T.) gondii

Published online by Cambridge University Press:  06 April 2009

A. W. C. A. Cornelissen
Affiliation:
Department of Tropical Veterinary Medicine and Protozoology, State University of Utrecht, P.O. Box 80172, 3508 TD Utrecht, The Netherlands
J. P. Overdulve
Affiliation:
Department of Tropical Veterinary Medicine and Protozoology, State University of Utrecht, P.O. Box 80172, 3508 TD Utrecht, The Netherlands
M. Van Der Ploeg
Affiliation:
Department of Histochemistry and Cytochemistry, Siate University of Leiden, Wassenaarseweg 72, 2333 AL Leiden, The Netherlands

Summary

DNA contents of individual stages of Isospora (Toxoplasma) gondii and other Eucoccida were measured after Feulgen-pararosaniline (SO2) staining either by direct microfluorometry or by scanning of microphotographic negatives. Frequency distributions were analysed using a computer program based on a mathematical model describing cell division. All stages of I. (T.) gondii, except fertilized macrogametes (2c), contained a haploid amount of DNA (1c), indicating that meiosis in I. (T.) gondii occurs during sporogony. Microgametes possessed 3·3% DNA in excess, presumably mitochondrial DNA. Nuclei of M2-and M3-merozoites differed in two characteristics: a small but distinct nucleolus was observed in almost 50% of the M2-merozoites but in none of the M3-merozoites; all M2 merozoites were strictly haploid, while all M3-merozoites were synthesizing DNA (17% above the haploid value). It may be concluded that all M2- and M3-merozoites are already sexually differentiated, i.e. are macro- and microgamontoblasts, respectively. DNA synthesis necessary for the development of the microgamont starts already in the microgamontoblast stage (M3-merozoite). M2-merozoites macrogametes, synthesize 11% extra DNA before fertilization, (after fertilization an extra amount of 12% of the diploid value was found), probably by amplification of genes for proteins which are needed for rapid maturation and later sporogony. Essentially parallel results have been found in Eimeria tenella and in crescent cystozoites of Sarcocystis cruzi. Absolute DNA values in representatives of the Eucoccida have been estimated as follows (10−15 g): I. (T.) gondii, 96; E. tenella and E. acervulina, both 75; S. cruzi, 216; Plasmodium berghei, 27. The value of the estimation of total haploid amounts as a tool in taxonomy of Eucoccida is discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1984

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

Bahr, G. F. (1966). Quantitative cytochemical study of erythrocytic stages of Plasmodium lophurae and Plasmodium berghei. Military Medicine 131, 1064–70.CrossRefGoogle Scholar
Bahr, G. F. & Mikel, U. (1972). The arrangement of DNA in the nucleus of rodent malaria parasites. Proceedings of the Helminthological Society (Washington) 39, 361–72.Google Scholar
Beyer, T. V. & Ovchinnikova, L. P. (1964). Cytophotometric study of RNA content in the macrogametogenesis of two rabbit intestinal coccidia Eimeria magna and E. intestinalis. Acta protozoologica 2, 329–37.Google Scholar
Böhm, N. (1968). Einfluss der Fixierung und der Säurekonzentration auf die Feulgen-Hydrolyse bei 28°C. Histochemie 14, 201–11.CrossRefGoogle Scholar
Böhm, N., Sprenger, E., Schlüter, G. & Sandritter, W. (1968). Proportionalitätsfehler bei der Feulgen-Hydrolyse. Histochemie 15, 194203.CrossRefGoogle 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
Bosman, F. T., Van Dee Ploeg, M., Van Duijn, P. & Schaberg, A. (1977 a). Photometric determination of the DNA distribution in the 24 human chromosomes. Experimental Cell Research 105, 301–11.CrossRefGoogle ScholarPubMed
Bosman, F. T., Van Der Ploeg, M. & Geraedts, J. P. M. (1977 b). Influence of Q-and G-banding on the Feulgen-stainability of human metaphase chromosomes. Histochemical Journal 9, 3142.CrossRefGoogle ScholarPubMed
Bosman, F. T., Van Dee Ploeg, M., Schaberg, A. & Van Duijn, P. (1975). Chromosome preparations of human blood lymphocytes-evaluation of techniques. Genetica 45, 425–33.CrossRefGoogle Scholar
Canning, E. U. (1962). Sexual differentiation of merozoites of Barrouxia schneideri (Bütschli). Nature 195, 720–1.CrossRefGoogle Scholar
Canning, E. U. (1973). Sexual differentiation in coccidia. In Progress in Protozoology. 4th International Congress on Protozoology, Clermont-Ferrand, p. 75.Google Scholar
Canning, E. U. & Anwar, M. (1968). Studies on meiotic division in coccidial and malarial parasites. Journal of Protozoology 15, 290–8.CrossRefGoogle ScholarPubMed
Canning, E. U. & Morgan, K. (1975). DNA synthesis, reduction, and elimination during life cycles of the eimeriine coccidian, Eimeria tenella and the haemogregarine, Hepatozoon domerguei. Experimental Parasitology 38, 217–27.CrossRefGoogle Scholar
Canning, E. U. & Sinden, R. E. (1973). The organization of the ookinete and observations on nuclear divisions in oocysts of Plasmodium berghei. Parasitology 67, 2940.CrossRefGoogle ScholarPubMed
Carter, R. & Diggs, C. L. (1977). Plasmodia of rodents. In Parasitic Protozoa, vol. 3 (ed. Kreier, J. P.), pp. 359465. New York, San Francisco and London: Academic Press.Google Scholar
Cheissin, E. M., Rosanov, J. M. & Kudryavtsev, B. N. (1968). Fluorescence microscopic study on the content of nucleic acids in merozoites and microgametes of Eimeria intestinalis from the intestine of rabbit. Acta protozoologica 5, 389–93.Google Scholar
Collins, W. E. & Aikawa, M. (1977). Plasmodia of non-human primates. In Parasitic Protozoa, vol. 3 (ed. Kreier, J. P.), pp. 467–92. New York, San Francisco and London: Academic Press.Google Scholar
Cornelissen, A. W. C. A. & Overdulve, J. P. (1980 a). Cytofluorimetrical determination of the DNA contents of stages of Isospora (Toxoplasma) gondii. Proceedings of the 3rd European Multicolloquium of Parasitology,September 7th-13th 1980,Cambridge, p. 21.Google Scholar
Cornelissen, A. W. C. A. & Overdulve, J. P. (1980 b). Sex determination and sex differentiation in coccidia: gametogony and oocyst production in cats infected with clones of Isospora (Toxoplasma) gondii. Proceedings of the 3rd European Multicolloquium of Parasitology,September 7th-13th 1980,Cambridge, p. 144.Google Scholar
Cornelissen, A. W. C. A. & Overdulve, J. P. (1981). Sex determination and sex differentiation in Isospora (Toxoplasma) gondii. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 594–6.CrossRefGoogle ScholarPubMed
Cornelissen, A. W. C. A. & Overdulve, J. P. (1982). Meiosis in coccidia: a quantitative cytophotometrical study on nuclear DNA of Isospora (Toxoplasma) gondii. Parasitology 84, xxxiii.Google Scholar
Cornelissen, A. W. C. A., Overdulve, J. P. & Van Der Ploeg, M. (1983). Cytochemical studies on nuclear DNA of four eucoccidian parasites, Isospora (Toxoplasma) gandii, Sarcocystis cruzi, Eimeria tenella and Plasmodium berghei. Parasitology 88, 1325.CrossRefGoogle Scholar
Den Tonkelaar, E. M. & Van Duijn, P. (1964). Photographic colorimetry as a quantitative cytochemical method. I. Principles and practice of the method. Histochemie 4, 19.CrossRefGoogle Scholar
Duijndam, W. A. L. & Van Duijn, D. (1975). The influence of chromatin compactness on the stoichiometry of the Feulgen–Schiff procedure studied in model films. II. Investigations on films containing condensed or swollen chicken erythrocyte nuclei. Journal of Histochemistry and Cytochemistry 23, 891900.CrossRefGoogle ScholarPubMed
Ferguson, D. J. P., Birch-Anderson, A., Hutchison, W. M. & SiiM, J. Chr. (1978). Light and electron microscopy on the sporulation of the oocysts of Eimeria brunetti. I. Development of the zygote and formation of the sporoblasts. Acta pathologica microbiologica scandinavica, Section B 86, 111.Google Scholar
Ferguson, D. J. P., Birch-Anderson, A., Siim, J. Chr. & Hutchison, W. M. (1979). Ultrastructural studies on the sporulation of oocysts of Toxoplasma gondii. I. Formation of the zygote and formation of the sporoblasts. Acta pathologica microbiologica scandinavica, Section B 87, 171–81.Google Scholar
Gaibova, G. D. (1972). Cytophotometric study of RNA content in growing macrogalnetes of Eimeria schamchorica and E. gliris (Sporozoa, Coccidia) (In Russian). Tsitologiya 14, 1529–34.Google Scholar
Garnham, P. C. C. (1966). Malaria Parasites and other Haemosporidia. Oxford: Blackwell Scientific Publications.Google Scholar
Geraedts, J. P. M. & Van Der Ploeg, M. (1980). DNA measurements of chromosomes 9 and 22 of six patients with t(9;22) and chronic myeloid leukemia. Cytometry 1, 152–5.CrossRefGoogle Scholar
Goldstein, D. J. (1981). Errors in microdensitometry. Histochemical Journal 13, 251–67.CrossRefGoogle ScholarPubMed
Hammond, D. M., Clark, W. N. & Miner, M. L. (1961). Endogenous phase of the life cycle of Eimeria auburnensis in calves. Journal of Parasitology 47, 591–6.CrossRefGoogle ScholarPubMed
Klimes, B., Rootes, O. G. & Tanielian, Z. (1972). Sexual differentiation of merozoites of Eimeria tenella. Parasitology 65, 131–6.CrossRefGoogle ScholarPubMed
Lee, E. H., Remmler, O. & Fernando, M. A. (1977). Sexual differentiation in Eimeria tenella. Journal of Parasitolgy 63, 155–6.CrossRefGoogle ScholarPubMed
McDougald, L. R. & Jeffers, T. K. (1976). Eimeria tenella (Sporozoa: Coccidia): gametogony following a single asexual generation. Science 192, 258–9.CrossRefGoogle ScholarPubMed
Mendelsohn, M. L., Mayal, B. H. (1974). Chromosome identification by image analysis and quantitative cytochemistry. In Human Chromosom Methodology (ed. Yunis, J. J.), pp. 311–46. New York and London: Academic Press.CrossRefGoogle Scholar
Nagl, W. (1976). Zellkern und Zellzyklen. Stuttgart: Ulmer.Google Scholar
Nagl, W. (1978). Endopolyploidy and Polyteny in Differentiation and Evolution. Amsterdam: North-Holland.Google Scholar
Overdulve, J. P. (1977). Taxonomy and hypotheses on the phylogony of Toxoplasma. Proceedings of the 5th International Congress of Protozoology, New York, p. 13.Google Scholar
Overdulve, J. P. (1978). Studies on the life cycle of Toxoplasma gondii in germfree, gnotobiotic and conventional cats. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Series C 81, 1959.Google Scholar
Overdulve, J. P. & Cornelissen, A. W. C. A. (1982). The DNA cycle in Eucoccida. Abstracts of the Vth International Congress of Parasitology, August 7th–14th 1982, Toronto. Molecular and Biochemical Parasitology, Suppl. 1982, 160.Google Scholar
Overdulve, J. P. & Cornelissen, A. W. C. A. (1983). Cytophotometric investigations on sexual and asexual multiplication of Sporozoa. Tropical and Geographical Medicine 35, 214–15.Google Scholar
Pellérdy, L. & Dürr, U. (1970). Zum endogenen Entwicklungszyklus von Eimeria stiedai (Clindeman, 1865) Kisskalt & Hartmann, 1907. Acta Veterinaria Academiae Scientiarum Hungaricae 20, 227–44.Google ScholarPubMed
Perrotto. J., Keister, D. B. & Gelderman, A. H. (1971). Incorporation of precursors into Toxoplasma DNA. Journal of Protozoology 18, 470–3.Google Scholar
Prenna, G., Leiva, S. & Mazzini, G. (1974). Quantitation of DNA by cytofluorometry of the conventional Feulgen reaction. Histochemical Journal 6, 467–89.CrossRefGoogle ScholarPubMed
Rutherford, R. L. (1943). The life cycle of four intestinal coccidia of the domestic rabbit. Journal of Parasitology 29, 1032.CrossRefGoogle Scholar
Scholtyseck, E. (1953). Beitrag zur Kenntnis des Entwicklungsganges des Hühnercoccids Eimeria tenella. Archiv für Protistenkunde 98, 415–65.Google Scholar
Scholtyseck, E. (1979). Fine Structure of Parasitic Protozoa. An Atlas of Micrographs, Drawings and Diagrams. Berlin, Heidelberg and New York: Springer.CrossRefGoogle Scholar
Shirley, M. W. & Millard, B. J. (1976). Some observation on the sexual differentiation of Eimeria tenella using single sporozoite infection in chicken embryos. Parasitology 73, 337–41.CrossRefGoogle ScholarPubMed
Sinden, R. E. (1978). Cell biology. In Rodent Malaria (ed. Killick-Kendrick, R. and Peters, W.), pp. 85168. London, New York and San Francisco: Academic Press.Google Scholar
Sitnden, R. E. (1982). Gametocytogenesis of Plasmodium falciparum in vitro: an electron microscopic study. Parasitology 84, 111.CrossRefGoogle Scholar
Sinden, R. E. & Smalley, M. E. (1979). Gametocytogenesis of Plasmodium falciparuin in vitro: the cell cycle. Parasitology 79, 277–96.CrossRefGoogle ScholarPubMed
Van Der Linden, P. M. (1980). Computer Analysis of DNA Histograms. Ph.D. thesis, Utrecht.Google Scholar
Van Der Ploeg, M., Van Den Broek, K., Smeulders, A. W. M., Vossepoel, A. M. & Van Duijn, P. (1977 a). Hidacsys: computer programs for interactive scanning cytophotometry. Histochemistry 54, 273–88.CrossRefGoogle ScholarPubMed
Van Der Ploeg, M., Van Duijn, P. & Ploem, J. S. (1974 a). High-resolution scanning-densitometry of photographic negatives of human metaphase chromosomes. I. Instrumentation. Histochemistry 42, 929.CrossRefGoogle ScholarPubMed
Van Der Ploeg, M., Van Duijn, P. & Ploem, J. S. (1974 b). High-resolution scanning-densitometry of photographic negatives of human metaphase chromosomes. II. Feulgen-DNA measurements. Histochemistry 42, 3146.CrossRefGoogle ScholarPubMed
Van Der Ploeg, M., Vossepoel, A. M., Bosman, F. Th. & Van Duijn, P. (1977 b). High-resolution scanning-densitometry of photographic negatives of human chromosomes. III. Determination of fluorescence emission intensities. Histochemistry 51, 269–91.CrossRefGoogle ScholarPubMed
Van Prooijen-Knegt, A. C., Redi, C. A. & Van Dee Ploeg, M. (1980). Quantitative aspects of the cytochemical Feulgen-DNA procedure studied on model systems and cell nuclei. Histochemistry 69, 117.CrossRefGoogle ScholarPubMed
Wagner, W. H. & Foerster, O. (1964). Die PAS-AO-Methode, eine Speziälfarbung für Coccidiën in Gewebe. Zeitschrift für Parasitenkunde 25, 2848.CrossRefGoogle Scholar
Wang, C. C. & Stotish, R. L. (1975). Changes of nucleic acids in the oocysts of Eimeria tenella during sporulation. Journal of Protozoology 22, 438–43.CrossRefGoogle Scholar