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Chromosome territory arrangement and homologous pairing in nuclei of Arabidopsis thaliana are predominantly random except for NOR-bearing chromosomes

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Abstract

Differential painting of all five chromosome pairs of Arabidopsis thaliana revealed for the first time the interphase chromosome arrangement in a euploid plant. Side-by-side arrangement of heterologous chromosome territories and homologous association of chromosomes 1, 3 and 5 (on average in 35–50% of nuclei) are in accordance with the random frequency predicted by computer simulations. Only the nucleolus organizing region (NOR)-bearing chromosome 2 and 4 homologs associate more often than randomly, since NORs mostly attach to a single nucleolus. Somatic pairing of homologous ∼100 kb segments occurs less frequently than homolog association, not significantly more often than expected at random and not simultaneously along the homologs. Thus, chromosome arrangement in Arabidopsis differs from that in Drosophila (characterized by somatic pairing of homologs), in spite of similar genome size, sequence organization and chromosome number. Nevertheless, in up to 31.5% of investigated Arabidopsis nuclei allelic sequences may share positions close enough for homologous recombination.

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References

  • Abranches R, Beven AF, Aragón-Alcaide L, Shaw PJ (1998) Transcriptional sites are not correlated with chromosome territories in wheat nuclei. J Cell Biol 143:5–12

    Article  CAS  PubMed  Google Scholar 

  • Aragón-Alcaide L, Reader S, Beven A, Shaw P, Miller T, Moore G (1997) Association of homologous chromosomes during floral development. Curr Biol 7:905–908

    Article  PubMed  Google Scholar 

  • Bickmore WA, Chubb JR (2003) Chromosome position: now where was I? Curr Biol 13:R357–R359

    Article  CAS  PubMed  Google Scholar 

  • Bridger JM, Boyle S, Kill IR, Bickmore WA (2000) Re-modelling of nuclear architecture in quiescent and senescent human fibroblasts. Curr Biol 10:149–152

    Article  CAS  PubMed  Google Scholar 

  • Burgess SM, Kleckner N, Weiner BM (1999) Somatic pairing of homologs in budding yeast: existence and modulation. Genes Dev 13:1627–1641

    CAS  PubMed  Google Scholar 

  • Chandley AC, Speed RM, Leitch AR (1996) Different distributions of homologous chromosomes in adult human Sertoli cells and in lymphocytes signify nuclear differentiation. J Cell Sci 109:773–776

    CAS  PubMed  Google Scholar 

  • Cornforth MN, Greulich-Bode KM, Loucas BD, Arsuaga J, Vásquez M, Sachs RK, Brückner M, Molls M, Hahnfeldt P, Hlatky L, Brenner DJ (2002) Chromosomes are predominantly located randomly with respect to each other in interphase human cells. J Cell Biol 159:237–244

    Article  CAS  PubMed  Google Scholar 

  • Cremer T, Cremer C (2001) Chromosome territories nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2:292–301

    Article  CAS  PubMed  Google Scholar 

  • Cremer M, von Hase J, Volm T, Brero A, Kreth G, Walter J, Fischer C, Solovei I, Cremer C, Cremer T (2001) Non-random radial higher-order chromatin arrangements in nuclei of diploid human cells. Chromosome Res 9:541–567

    Article  CAS  PubMed  Google Scholar 

  • Csink AK, Henikoff S (1998) Large-scale chromosomal movements during interphase progression in Drosophila. J Cell Biol 143:13–22

    Article  CAS  PubMed  Google Scholar 

  • Dong F, Jiang J (1998) Non-Rabl patterns of centromere and telomere distribution in the interphase nuclei of plant cells. Chromosome Res 6:551–558

    Article  CAS  PubMed  Google Scholar 

  • Fransz P, de Jong JH, Lysak MA, Ruffini-Castiglione M, Schubert I (2002) Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc Natl Acad Sci USA 99:14584–14589

    Article  CAS  PubMed  Google Scholar 

  • Fuchs J, Houben A, Brandes A, Schubert I (1996) Chromosome ‘painting’ in plants—a feasible technique? Chromosoma 104:315–320

    Article  CAS  PubMed  Google Scholar 

  • Fuchs J, Lorenz A, Loidl J (2002) Chromosome associations in budding yeast caused by integrated tandemly repeated transgenes. J Cell Sci 115:1213–1220

    CAS  PubMed  Google Scholar 

  • Fung JC, Marshall WF, Dernburg A, Agard DA, Sedat JW (1998) Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations. J Cell Biol 141:5–20

    Article  CAS  PubMed  Google Scholar 

  • Gerlich D, Beaudouin J, Kalbfuss B, Daigle N, Eils R, Ellenberg J (2003) Global chromosome positions are transmitted through mitosis in mammalian cells. Cell 112:751–764

    Article  CAS  PubMed  Google Scholar 

  • Habermann FA, Cremer M, Walter J, Kreth G, von Hase J, Bauer K, Wienberg J, Cremer C, Cremer T, Solovei I (2001) Arrangements of macro- and microchromosomes in chicken cells. Chromosome Res 9:569–584

    Article  CAS  PubMed  Google Scholar 

  • Heitz E (1928) Heterochromatin der Moose I. Jahrb Wiss Bot 69:762–818

    Google Scholar 

  • Henegariu O, Bray-Ward P, Ward DC (2000) Custom fluorescent-nucleotide synthesis as an alternative method for nucleic acid labeling. Nat Biotechnol 18:345–348

    Article  CAS  PubMed  Google Scholar 

  • Hiraoka Y, Dernburg AF, Parmelee SJ, Rykowski MC, Agard DA, Sedat JW (1993) The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis. J Cell Biol 120:591–600

    Article  CAS  PubMed  Google Scholar 

  • Kato N, Lam E (2003) Chromatin of endoreduplicated pavement cells has a greater range of movement than that of diploid guard cells in Arabidopsis thaliana. J Cell Sci 116:2195–2201

    Article  CAS  PubMed  Google Scholar 

  • Kozubek S, Lukášová E, Jirsová P, Koutná I, Kozubek M, Ganová A, Bártová E, Falk M, Paseková R (2002) 3D structure of the human genome: order in randomness. Chromosoma 111:321–331

    CAS  PubMed  Google Scholar 

  • Kreth G, Finsterle J, Hase J von, Cremer M, Cremer C (2004) Radial arrangement of chromosome territories in human cell nuclei: a computer model approach based on gene density indicates a probabilistic global positioning code. Biophys J 86:2803–2812

    CAS  PubMed  Google Scholar 

  • Lam E, Kato N, Watanabe K (2004) Visualizing chromosome structure/organization. Annu Rev Plant Biol 55:537–554

    Article  CAS  PubMed  Google Scholar 

  • Lichter P, Cremer T, Borden J, Manuelidis L, Ward DC (1988) Delineation of individual human chromosomes in metaphase and interphase cells by in situ suppression hybridization using recombinant DNA libraries. Hum Genet 80:224–234

    CAS  PubMed  Google Scholar 

  • Lorenz A, Fuchs J, Bürger R, Loidl J (2003) Chromosome pairing does not contribute to nuclear architecture in vegetative yeast cells. Eukaryot Cell 2:856–866

    Article  CAS  PubMed  Google Scholar 

  • Lysak MA, Fransz PF, Ali HBM, Schubert I (2001) Chromosome painting in Arabidopsis thaliana. Plant J 28:689–697

    Article  CAS  PubMed  Google Scholar 

  • Lysak MA, Pecinka A, Schubert I (2003) Recent progress in chromosome painting of Arabidopsis and related species. Chromosome Res 11:195–204

    Article  CAS  PubMed  Google Scholar 

  • Mahy NL, Perry PE, Gilchrist S, Baldock RA, Bickmore WA (2002a) Spatial organization of active and inactive genes and noncoding DNA within chromosome territories. J Cell Biol 157:579–589

    Article  CAS  PubMed  Google Scholar 

  • Mahy NL, Perry PE, Bickmore WA (2002b) Gene density and transcription influence the localization of chromatin outside of chromosome territories detectable by FISH. J Cell Biol 159:753–763

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Pérez E, Shaw P, Moore G (2001) The Ph1 locus is needed to ensure specific somatic and meiotic centromere association. Nature 411:204–207

    Article  PubMed  Google Scholar 

  • McKee BD (2004) Homologous pairing and chromosome dynamics in meiosis and mitosis. Biochim Biophys Acta 1677:165–180

    Article  CAS  PubMed  Google Scholar 

  • Metropolis N, Rosenbluth AW, Rosenbluth MN, Teller AH, Teller E (1953) Equation of state calculations by fast computing machines. J Chem Phys 21:1087–1092

    CAS  Google Scholar 

  • Nagele RG, Freeman T, McMorrow L, Thomson Z, Kitson-Wind K, Lee H-Y (1999) Chromosomes exhibit preferential positioning in nuclei of quiescent human cells. J Cell Sci 112:525–535

    CAS  PubMed  Google Scholar 

  • Parada LA, Misteli T (2002) Chromosome positioning in the interphase nucleus. Trends Cell Biol 12:425–432

    Article  CAS  PubMed  Google Scholar 

  • Parada LA, Roix JJ, Misteli T (2003) An uncertainty principle in chromosome positioning. Trends Cell Biol 13:393–396

    Article  CAS  PubMed  Google Scholar 

  • Pinkel D, Landegent J, Collins C, Fuscoe J, Segraves R, Lucas J, Gray J (1988) Fluorescence in situ hybridization with human chromosome-specific libraries: detection of trisomy 21 and translocations of chromosome 4. Proc Natl Acad Sci USA 85:9138–9142

    CAS  PubMed  Google Scholar 

  • Prieto P, Santos AP, Moore G, Shaw P (2004) Chromosomes associate premeiotically and in xylem vessel cells via their telomeres and centromeres in diploid rice (Oryza sativa). Chromosoma 112:300–307

    Article  PubMed  Google Scholar 

  • Rabl C (1885) Über Zelltheilung. Morphol Jahrbuch 10:214–330

    Google Scholar 

  • Rieger R, Michaelis A, Schubert I, Meister A (1973) Somatic interphase pairing of Vicia chromosomes as inferred from the hom/het ratio of induced chromatid interchanges. Mutat Res 20:295–298

    Article  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, vol 1, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Schubert I, Rieger R, Fuchs J, Pich U (1994) Sequence organization and the mechanism of interstitial deletion clustering in a plant genome (Vicia faba). Mutat Res 325:1–5

    Article  CAS  PubMed  Google Scholar 

  • Schubert I, Shi F, Fuchs J, Endo TR (1998) An efficient screening for terminal deletions and translocations of barley chromosomes added to common wheat. Plant J 14:489–495

    Article  CAS  Google Scholar 

  • Schubert I, Fransz PF, Fuchs J, de Jong JH (2001) Chromosome painting in plants. Methods Cell Sci 23:57–69

    Article  CAS  PubMed  Google Scholar 

  • Schubert I, Pecinka A, Meister A, Schubert V, Klatte M, Jovtchev G (2004) DNA damage processing and aberration formation in plants. Cytogenet Genome Res 104:104–108

    Article  CAS  PubMed  Google Scholar 

  • Schwarzacher T, Leitch AR, Bennett MD, Heslop-Harrison JS (1989) In situ localization of parental genomes in a wide hybrid. Ann Bot 64:315–324

    Google Scholar 

  • Schwarzacher T, Anamthawat-Jonsson K, Harrison GE, Islam AKMR, Jia JZ, King IP, Leitch AR, Miller TE, Reader SM, Rogers WJ et al (1992) Genomic in situ hybridization to identify alien chromosomes and chromosome segments in wheat. Theor Appl Genet 84:778–786

    Google Scholar 

  • Soppe WJJ, Jacobsen SE, Alonso-Blanco C, Jackson JB, Kakutani T, Koornneef M, Peeters AJM (2000) The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell 6:791–802

    CAS  PubMed  Google Scholar 

  • Tanabe H, Müller S, Neusser M, von Hase J, Calcagno E, Cremer M, Solovei I, Cremer C, Cremer T (2002) Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates. Proc Natl Acad Sci USA 99:4424–4429

    Article  CAS  PubMed  Google Scholar 

  • The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  PubMed  Google Scholar 

  • Volpi EV, Chevret E, Jones T, Vatcheva R, Williamson J, Beck S, Campbell RD, Goldsworthy M, Powis SH, Ragoussis J, Trowsdale J, Sheer D (2000) Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J Cell Sci 113:1565–1576

    CAS  PubMed  Google Scholar 

  • Walter J, Schmelleh L, Cremer M, Tashiro S, Cremer T (2003) Chromosome order in HeLa cells changes during mitosis and early G1 but is stably maintained during subsequent interphase stages. J Cell Biol 160:685–697

    Article  CAS  PubMed  Google Scholar 

  • Ward PB (2002) FISH probes and labelling techniques. In: Beatty B, Mai S, Squire J (eds) FISH. Oxford University, Oxford, pp 5–28

    Google Scholar 

  • Williams RRE, Fisher AG (2003) Chromosomes positions please! Nat Cell Biol 5:388–390

    Article  CAS  PubMed  Google Scholar 

  • Zink D, Cremer T, Saffrich R, Fischer R, Trendelenburg MF, Ansorge W, Stelzer EHK (1998) Structure and dynamics of human interphase chromosome territories in vivo. Hum Genet 102:241–251

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank C. Cremer for many helpful discussions and for support with modeling of Arabidopsis chromosome territories, Z. Jasencakova for unpublished results on FISH data for 45S rDNA in Arabidopsis nuclei of different ploidy level, R. Rieger for critical reading of the manuscript, A. Houben and the anonymous referees for helpful comments, and R. Schubert, M. Kühne and J. Bruder for technical assistance. This work was supported by the Deutsche Forschungsgemeinschaft (Schu 951/10-1, Ly 19/1-1 and Cr 60/19-1).

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  1. Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstrasse 3, 06466, Gatersleben, Germany

    Ales Pecinka, Veit Schubert, Armin Meister, Marco Klatte, Martin A. Lysak, Jörg Fuchs & Ingo Schubert

  2. Kirchhoff Institute for Physics, University of Heidelberg, 69120, Heidelberg, Germany

    Gregor Kreth

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  1. Ales Pecinka
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Correspondence to Ingo Schubert.

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Communicated by E.A. Nigg

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Pecinka, A., Schubert, V., Meister, A. et al. Chromosome territory arrangement and homologous pairing in nuclei of Arabidopsis thaliana are predominantly random except for NOR-bearing chromosomes. Chromosoma 113, 258–269 (2004). https://doi.org/10.1007/s00412-004-0316-2

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