Organization and pairing of meiotic chromosomes in the ciliate Tetrahymena thermophila

Journal of Cell Science

Volumn 117, Issue 24, 2004, Pages 5791-5801

  Loidl, Josef ^a   Scherthan, Harry ^b  

^a UNIVERSITY OF VIENNA   (Austria)

^b Bundeswehr Institute for Radiation Biology   (Germany)

Author keywords

Chromosome pairing; Meiosis; Protists; Rad51; Recombination

Indexed keywords

BROXURIDINE; DOUBLE STRANDED DNA; RAD51 PROTEIN;

ARTICLE; CHROMATIN; CHROMOSOME CHIASM; CHROMOSOME PAIRING; CHROMOSOME STRUCTURE; CILIATE; CROSSING OVER; DNA STRAND BREAKAGE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE LOCUS; GENETIC RECOMBINATION; IMMUNOHISTOCHEMISTRY; KARYOTYPE; MEIOSIS; MICRONUCLEUS; NONHUMAN; PRIORITY JOURNAL; PROPHASE; PROTEIN LOCALIZATION; PROTOZOAL GENETICS; SEQUENCE HOMOLOGY; SYNAPTONEMAL COMPLEX; TELOMERE; TETRAHYMENA THERMOPHILA;

ANIMALS; BROMODEOXYURIDINE; CELL NUCLEUS; CHROMOSOMES; COLORING AGENTS; DNA DAMAGE; DNA-BINDING PROTEINS; IN SITU HYBRIDIZATION; IN SITU HYBRIDIZATION, FLUORESCENCE; MEIOSIS; MICRONUCLEI, CHROMOSOME-DEFECTIVE; MODELS, BIOLOGICAL; MUTATION; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; SILVER STAINING; TETRAHYMENA THERMOPHILA; TIME FACTORS;

CILIOPHORA; PROTISTA; PROTOZOA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

EID: 12344282204     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01504     Document Type: Article

References (70)

1. Allis, C. D., Colavito-Shepanski, M. and Gorovsky, M. A. (1987). Scheduled and unscheduled DNA synthesis during development in conjugating Tetrahymena. Dev. Biol. 124, 469-480.
2. Alpi, A., Pasierbek, P., Gartner, A. and Loidl, J. (2003). Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans. Chromosoma 112, 6-16.
3. Alsheimer, M., von Glasenapp, E., Hock, R. and Benavente, R. (1999). Architecture of the nuclear periphery of rat pachytene spermatocytes: distribution of nuclear envelope proteins in relation to synaptonemal complex attachment sites. Mol. Biol. Cell 10, 1235-1245.
4. Bass, H. W. (2003). Telomere dynamics unique to meiotic prophase: formation and significance of the bouquet. Cell Mol. Life Sci. 60, 2319-2324.
5. Bass, H. W., Riera-Lizarazu, O., Ananiev, E. V., Bordoli, S. J., Rines, H. W., Phillips, R. L., Sedat, J. W., Agard, D. A. and Cande, W. Z. (2000). Evidence for the coincident initiation of homolog pairing and synapsis during the telomere-clustering (bouquet) stage of meiotic prophase. J. Cell Sci. 113, 1033-1042.
6. Bähler, J., Wyler, T., Loidl, J. and Kohli, J. (1993). Unusual nuclear structures in meiotic prophase of fission yeast: a cytological analysis. J. Cell Biol. 121, 241-256.
7. Börner, G. V., Kleckner, N. and Hunter, N. (2004). Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117, 29-45.
8. Bruns, P. J., Brussard, T. B. and Merriam, E. V. (1982). In vitro genetic engineering in Tetrahymena. In Progress in Protozoology (Proc. VI. Int. Congr. Protozool.), Acta Protozool. special congress volume, Part I (ed. S. Dryl, S. L. Kazubski, L. Kuznicki and J. Ploszai), pp. 31-44. Stuttgart, Germany: Fischer Verlag.
9. Brush, G. S. (2002). Recombination functions of replication protein A. Curr. Org. Chem. 6, 795-813.
10. Chikashige, Y. and Hiraoka, Y. (2001). Telomere binding of the Rap1 protein is required for meiosis in fission yeast. Curr. Biol. 11, 1618-1623.
11. Chikashige, Y., Ding, D.-Q., Funabiki, H., Haraguchi, T., Mashiko, S., Yanagida, M. and Hiraoka, Y. (1994). Telomere-led premeiotic chromosome movement in fission yeast. Science 264, 270-273.
12. Chikashige, Y., Ding, D.-Q., Imai, Y., Yamamoto, M., Haraguchi, T. and Hiraoka, Y. (1997). Meiotic nuclear reorganization: switching the position of centromeres and telomeres in the fission yeast Schizosaccharomyces pombe. EMBO J. 16, 193-202.
13. Chua, P. R. and Roeder, G. S. (1997). Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev. 11, 1786-1800.
14. Colaiácovo, M. P., MacQueen, A. J., Martinez-Perez, E., McDonald, K., Adamo, A., la Volpe, A. and Villeneuve, A. M. (2003). Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev. Cell 5, 463-474.
15. Cole, E. S., Cassidy-Hanley, D., Hemish, J., Tuan, J. and Bruns, P. J. (1997). A mutational analysis of conjugation in Tetrahymena thermophila. 1. Phenotypes affecting early development: meiosis to nuclear selection. Dev. Biol. 189, 215-232.
16. Cowan, C. R., Carlton, P. M. and Cande, W. Z. (2001). The polar arrangement of telomeres in interphase and meiosis. Rabl organization and the bouquet. Plant Physiol. 125, 532-538.
17. Davidson, L. and LaFountain, J. R., Jr (1975). Mitosis and early meiosis in Tetrahymena pyriformis and the evolution of mitosis in the phylum Ciliophora. BioSystems 7, 326-336.
18. Deak, J. C. and Doerder, F. P. (1998). High frequency intragenic recombination during macronuclear development in Tetrahymena thermophila restores the wild-type SerH1 gene. Genetics 148, 1109-1115.
19. Ding, D.-Q., Chikashige, Y., Haraguchi, T. and Hiraoka, Y. (1998). Oscillatory nuclear movement in fission yeast meiotic prophase is driven by astral microtubules, as revealed by continuous observation of chromosomes and microtubules in living cells. J. Cell Sci. 111, 701-712.
20. Ding, D.-Q., Yamamoto, A., Haraguchi, T. and Hiraoka, Y. (2004). Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev. Cell 6, 329-341.
21. Dorninger, D., Karigl, G. and Loidl, J. (1995). Simulation of chromosomal homology searching in meiotic pairing. J. Theor. Biol. 176, 247-260.
22. Egel-Mitani, M., Olson, L. W. and Egel, R. (1982). Meiosis in Aspergillus nidulans: another example for lacking synaptonemal complexes in the absence of crossover interference. Hereditas 97, 179-187.
23. Fletcher, H. L. (1981). A search for synaptonemal complexes in Ustilago maydis. J. Cell Sci. 50, 171-180.
24. Frankel, J. (2000). Cell biology of Tetrahymena thermophila. In Tetrahymena thermophila (ed. D. J. Asai and J. D. Forney), pp. 27-125. San Diego, CA: Academic Press.
25. Fung, J. C., Rockmill, B., Odell, M. and Roeder, G. S. (2004). Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116, 795-802.
26. Gaertig, J. and Fleury, A. (1992). Spatio-temporal reorganization of intracytoplasmic microtubules is associated with nuclear selection and differentiation during the developmental process in the ciliate Tetrahymena thermophila. Protoplasma 167, 74-87.
27. García-Rubio, M., Huertas, P., González-Barrera, S. and Aguilera, A. (2003). Recombinogenic effects of DNA-damaging agents are synergistically increased by transcription in Saccharomyces cerevisiae: new insights into transcription-associated recombination. Genetics 165, 457-466.
28. Haldane, J. B. S. (1931). The cytological basis of genetical interference. Cytologia 3, 54-65.
29. Jones, G. H. (1984). The control of chiasma distribution. In Controlling events in meiosis (ed. C. W. Evans and H. G. Dickinson), pp. 293-320. Cambridge: Company of Biologists.
30. Kaczanowski, A., Gaertig, J. and Kubiak, J. (1985). Effect of the antitubulin drug nocodazole on meiosis and postmeiotic development in Tetrahymena thermophila. Induction of achiasmatic meiosis. Exp. Cell Res. 158, 244-256.
31. Karrer, K. M. (1985). Nonrandom localization of DNA sequences in the crescent micronucleus of Tetrahymena. J. Protozool. 32, 555-557.
32. Karrer, K. M. (2000). Tetrahymena genetics: two nuclei are better than one. In Tetrahymena thermophila (ed. D. J. Asai and J. D, Forney), pp. 127-186. San Diego: Academic Press.
33. Kirk, K. E. and Blackburn, E. H. (1995). An unusual sequence arrangement in the telomeres of the germ-line micronucleus in Tetrahymena thermophila. Genes Dev. 9, 59-71.
34. Kohli, J. and Bähler, J. (1994). Homologous recombination in fission yeast - absence of crossover interference and synaptonemal complex. Experientia 50, 295-306.
35. Loidl, J. (1990). The initiation of meiotic chromosome pairing: the cytological view. Genome 33, 759-778.
36. Loidl, J. (1994). Cytological aspects of meiotic recombination. Experientia 50, 285-294.
37. Loidl, J., Klein, F. and Engebrecht, J. (1998). Genetic and morphological approaches for the analysis of meiotic chromosomes in yeast. In Nuclear structure and function (ed. M. Berrios), pp. 257-285. San Diego, CA: Academic Press.
38. Maercker, C., Kortwig, H., Nikiforov, M. A., Allis, C. D. and Lipps, H. J. (1999). A nuclear protein involved in apoptotic-like DNA degradation in Stylonychia: implications for similar mechanisms in differentiating and starved cells. Mol. Biol. Cell 10, 3003-3014.
39. Maguire, M. P. (1988). Crossover site determination and interference. J. Theor. Biol. 134, 565-570.
40. Marsh, T. C., Cole, E. S., Stuart, K. R., Campbell, C. and Romero, D. P. (2000). RAD51 is required for propagation of the germinal nucleus in Tetrahymena thermophila. Genetics 154, 1587-1596.
41. Martindale, D. W., Allis, C. D. and Bruns, P. J. (1982). Conjugation in Tetrahymena thermophila. A temporal analysis of cytological stages. Exp. Cell Res. 140, 227-236.
42. Martindale, D. W., Allis, C. D. and Bruns, P. J. (1985). RNA and protein synthesis during meiotic prophase in Tetrahymena thermophila. J. Protozool. 32, 644-649.
43. Moens, P. B., Bernelot-Moens, C. and Spyropoulos, B. (1989). Chromosome core attachment to the meiotic nuclear envelope regulates synapsis in Chloealtis (Orthoptera). Genome 32 601-610.
44. Nanney, D. L. and McCoy, J. W. (1976). Characterization of the species of the Tetrahymena pyriformis complex. Trans. Am. Microsc. Soc. 95, 664-682.
45. Novak, J. E., Ross-Macdonald, P. B. and Roeder, G. S. (2001). The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158, 1013-1025.
46. Olson, L. W., Edén, U., Mitani, M. E. and Egel, R. (1978). Asynaptic meiosis in fission yeast? Hereditas 89, 189-199.
47. Orias, E., Hamilton, E. P. and Orias, J. D. (2000). Tetrahymena as a laboratory organism: useful strains, cell culture, and cell line maintenance. In Tetrahymena thermophila (ed. D. J. Asai and J. D. Forney), pp. 189-211. San Diego: Academic Press.
48. Page, S. L. and Hawley, R. S. (2001). c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev. 15, 3130-3143.
49. Paques, F. and Haber, J. E. (1999). Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63, 349-404.
50. Pawlowski, W. P., Golubovskaya, I. N. and Cande, W. Z. (2003). Altered nuclear distribution of recombination protein RAD51 in maize mutants suggests the involvement of RAD51 in meiotic homology recognition. Plant Cell 15, 1807-1816.
51. Raikov, I. B. (1982). The Protozoan Nucleus. Morphology and Evolution, pp. 1-474. New York, NY: Springer-Verlag.
52. Ray, C., Jr (1956). Meiosis and nuclear behaviour in Tetrahymena pyriformis. J. Protozool. 3, 88-96.
53. Roeder, G. S. (1997). Meiotic chromosomes: it takes two to tango. Genes Dev. 11, 2600-2621.
54. Scherthan, H. (2001). A bouquet makes ends meet. Nat. Rev. Mol. Cell Biol. 2, 621-627.
55. Scherthan, H. (2002). Detection of chromosome ends by telomere FISH. Methods Mol. Biol. 191, 13-31.
56. Scherthan, H., Weich, S., Schwegler, H., Härler, M., Heyting, C. and Cremer, T. (1996). Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J. Cell Biol. 134, 1109-1125.
57. Shinohara, A., Ogawa, H. and Ogawa, T. (1992). RAD51 Protein involved in repair and recombination in Saccharomyces cerevisiae is a RECA-like protein. Cell 69, 457-470.
58. Stechmann, A. and Cavalier-Smith, T. (2003). The root of the eukaryote tree pinpointed. Curr. Biol. 13, R665-R666.
59. Storlazzi, A., Tesse, S., Gargano, S., James, F., Kleckner, N. and Zickler, D. (2003). Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division. Genes Dev. 17, 2675-2687.
60. Sugai, T. and Hiwatashi, K. (1974). Cytologic and autoradiographic studies of the micronucleus at meiotic prophase in Tetrahymena pyriformis. J. Protozool. 21, 542-548.
61. Sung, P., Krejci, L., van Komen, S. and Sehorn, M. G. (2003). Rad51 recombinase and recombination mediators. J. Biol. Chem. 278, 42729-42732.
62. Sym, M. and Roeder, G. S. (1994). Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79, 283-292.
63. Tung, K.-S. and Roeder, G. S. (1998). Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae. Genetics 149, 817-832.
64. Wei, Y., Mizzen, C. A., Cook, R. G., Gorovsky, M. A. and Allis, C. D. (1998). Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc. Natl. Acad. Sci. USA 95, 7480-7484.
65. Wickert, S. and Orias, E. (2000). Tetrahymena micronuclear genome mapping: a high-resolution meiotic map of chromosome 1L. Genetics 154, 1141-1153.
66. Wolfe, J., Hunter, B. and Adair, W. S. (1976). A cytological study of micronuclear elongation during conjugation in Tetrahymena. Chromosoma 55, 289-308.
67. Yamamoto, A. and Hiraoka, Y. (2001). How do meiotic chromosomes meet their homologous partners?: lessons from fission yeast. BioEssays 23, 526-533.
68. Zickler, D. and Kleckner, N. (1998). The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32 619-697.
69. Zickler, D. and Kleckner, N. (1999). Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33, 603-754.
70. Zink, D., Cremer, T., Saffrich, R., Fischer, R., Trendelenburg, M. F., Ansorge, W. and Stelzer, E. H. K. (1998). Structure and dynamics of human interphase chromosome territories in vivo. Hum. Genet. 102, 241-251.