Abstract
Homologue pairing mediates both recombination and segregation of chromosomes at meiosis I. The recognition of nucleic-acid-sequence homology within the somatic nucleus has an impact on DNA repair and epigenetic control of gene expression. Here we investigate interchromosomal interactions using a non-invasive technique that allows tagging and visualization of DNA sequences in vegetative and meiotic live yeast cells. In non-meiotic cells, chromosomes are ordered in the nucleus, but preferential pairing between homologues is not observed. Association of tagged chromosomal domains occurs irrespective of their genomic location, with some preference for similar chromosomal positions. Here we describe a new phenomenon that promotes associations between sequence-identical ectopic tags with a tandem-repeat structure. These associations, termed interchromosome trans-associations, may underlie epigenetic phenomena.
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References
Csink, A. K. & Henikoff, S. Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature 381, 529–531 (1996).
Dorer, D. R. & Henikoff, S. Transgene repeat arrays interact with distant heterochromatin and cause silencing in cis and trans. Genetics 147, 1181–1190 (1997).
Lichten, M. & Haber, J. E. Position effects in ectopic and allelic mitotic recombination in Saccharomyces cerevisiae. Genetics 123, 261–268 (1989).
Kassis, J. A., VanSickle, E. P. & Sensabaugh, S. M. A fragment of engrailed regulatory DNA can mediate transvection of the white gene in Drosophila. Genetics 128, 751–761 (1991).
Haber, J. E. et al. Physical monitoring of meiotic and mitotic recombination in yeast. Prog. Nucleic Acids Res. Mol. Biol. 35, 209–259 (1988).
Loidl, J., Klein, F. & Scherthan, H. Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J. Cell Biol. 125, 1191–1200 (1994).
Weiner, B. M. & Kleckner, N. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77, 977–991 (1994).
Scherthan, H., Bahler, J. & Kohli, J. Dynamics of chromosome organization and pairing during meiotic prophase in fission yeast. J. Cell Biol. 127, 273–285 (1994).
Burgess, S. M., Kleckner, N. & Weiner, B. M. Somatic pairing of homologs in budding yeast: existence and modulation. Genes Dev. 13, 1627–1641 (1999).
Bass, H. W., Marshall, W. F., Sedat, J. W., Agard, D. A. & Cande, W. Z. Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. J. Cell Biol. 137, 5–18 (1997).
Scherthan, H. et al. 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 (1996).
Kleckner, N. & Weiner, B. M. Potential advantages of unstable interactions for pairing of chromosomes in meiotic, somatic, and premeiotic cells. Cold Spring Harb. Symp. Quant. Biol. 58, 553–565 (1993).
Burgess, S. M. & Kleckner, N. Collisions between yeast chromosomal loci in vivo are governed by three layers of organisation. Genes Dev. 13, 1871–1883 (1999).
Guacci, V., Hogan, E. & Koshland, D. Centromere position in budding yeast: evidence for anaphase A. Mol. Biol. Cell 8, 957–972 (1997).
Jin, Q., Trelles-Sticken, E., Scherthan, H. & Loidl, J. Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase. J. Cell Biol. 141, 21–29 (1998).
Gotta, M. et al. The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae. J. Cell Biol. 134, 1349–1363 (1996).
Straight, A. F., Belmont, A. S., Robinett, C. C. & Murray, A. W. GFP tagging of budding yeast chromosomes reveals that protein–protein interactions can mediate sister chromatid cohesion. Curr. Biol. 6, 1599–1608 (1996).
Michaelis, C., Ciosk, R. & Nasmyth, K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35–45 (1997).
Bishop, D. K., Park, D., Xu, L. & Kleckner, N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69, 439–456 (1992).
Li, G., Sudlow, G. & Belmont, A. S. Interphase cell cycle dynamics of a late-replicating, heterochromatic homogeneously staining region: precise choreography of condensation/decondensation and nuclear positioning. J. Cell Biol. 140, 975–989 (1998).
Mitchell, A. P. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol. Rev. 58, 56–70 (1994).
Haber, J. E., Ray, B. L., Kolb, J. M. & White, C. I. Rapid kinetics of mismatch repair of heteroduplex DNA that is formed during recombination in yeast. Proc. Natl Acad. Sci. USA 90, 3363–3367 (1993).
Jinks-Robertson, S., Michelitch, M. & Ramcharan, S. Substrate length requirements for efficient mitotic recombination in Saccharomyces cerevisiae. Mol. Cell Biol. 13, 3937–3950 (1993).
Inbar, O. & Kupiec, M. Homology search and choice of homologous partner during mitotic recombination. Mol. Cell Biol. 19, 4134–4142 (1999).
Melamed, C. & Kupeiec, M. Effect of donor copy number on the rate of gene conversion in the yeast Saccharomyces cerevisiae. Mol. Gen. Genet. 235, 97–103 (1992).
Haber, J. E. & Leung, W. Lack of chromosome territoriality in yeast: promiscuous rejoining of broken chromosome ends. Proc. Natl Acad. Sci. USA 93, 13949–13954 (1996).
Wolffe, A. & Matzke, M. A. Epigenetics: regulation through repression. Science 286, 481–486 (1999).
Henikoff, S. Nuclear organization and gene expression: homologous pairing and long-range interactions. Curr. Opin. Cell Biol. 9, 388–395 (1997).
Jinks-Robertson, S. & Petes, T. D. Chromosomal trans-locations generated by high-frequency meiotic recombination between repeated yeast genes. Genetics 114, 731–752 (1986).
Lewis, M. et al. Crystal structure of the lactose operon repressor and its complexes with DNA and inducer. Science 271, 1247–1254 (1996).
Lewis, E. B. The theory and application of a new method of detecting chromosomal rearrangements in Drosophila melanogaster. Am. Nat. 88, 225–239 (1954).
Judd, B. H. Transvection: allelic cross talk. Cell 53, 841–843 (1988).
Wassenegger, M. & Pelissier, T. A model for RNA-mediated gene silencing in higher plants. Plant Mol. Biol. 37, 349–362 (1998).
Cogoni, C. & Macino, G. Isolation of quelling-defective (qde) mutants impaired in posttranscriptional transgene-induced gene silencing in Neurospora crassa. Proc. Natl Acad. Sci. USA 94, 10233–10238 (1997).
Tabara, H., Grishok, A. & Mello, C. C. RNAi in C. elegans: soaking in the genome sequence. Science 282, 430–431 (1998).
Selker, E. U. Epigenetic phenomena in filamentous fungi: useful paradigms or repeat-induced confusion? Trends Genet. 13, 296–301 (1997).
Rossignol, J. L. & Faugeron, G. MIP: an epigenetic gene silencing process in Ascobolus immersus. Curr. Top. Microbiol. Immunol. 197, 179–191 (1995).
Ito, H., Fukuda, Y., Murata, K. & Kimura, A. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163–168 (1983).
Sikorski, R. S. & Hieter, P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19–27 (1989).
Mumberg, D., Muller, R. & Funk, M. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156, 119–122 (1995).
Freeman, L., Aragón-Alcaide, L. & Strunnikov, A. The condesin complex governs chromosome condensation and mitotic transmission of rDNA. J. Cell Biol. 149, 811–824 (2000).
Acknowledgements
We thank M. Lichten, A. Straight, A. Murray, D. Koshland and K. Nasmyth for research materials, and A. Wolffe, E. Ballestar, M. Dasso, O. Cohen-Fix, L. Freeman, F. Urnov, C. P. Lichtestein and A. R. Leitch for ideas and comments on the manuscript. L.A-A. was supported by the NICHD Intramural Research Training Award and in part by the BBSRC.
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Aragón-Alcaide, L., Strunnikov, A. Functional dissection of in vivo interchromosome association in Saccharomyces cerevisiae. Nat Cell Biol 2, 812–818 (2000). https://doi.org/10.1038/35041055
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DOI: https://doi.org/10.1038/35041055
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