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Similar rye A and B chromosome organization in meristematic and differentiated interphase nuclei

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Abstract

Supernumerary (B) chromosomes of rye are not required for plant development and exhibit a reduced transcription activity. These special features inspired us to analyse whether there are differences between A and B chromatin organization in interphase nuclei. Applying fluorescence in situ hybridization, we found that both rye A and B chromosomes added to hexaploid wheat showed in meristematic nuclei a string-like shape and a clear Rabl orientation. In 4C differentiated leaf nuclei, a more relaxed chromatin structure, round-shaped chromosome territories and a less pronounced Rabl configuration were found. Also, the observed random association of homologues in 2C and 4C nuclei indicated in general a similar behaviour of A and B chromosomes. Whereas in differentiated 4C nuclei A sister centromeres are separated, B sister centromeres align in nearly all nuclei. In short, despite the different transcription activity of A and B chromosomes, both types of chromosomes exhibit a similar organization in meristematic and differentiated interphase nuclei. But the deletion of a B chromosome segment responsible for non-disjunction during gametogenesis induces released sister centromeres also in some interphase nuclei of somatic tissue. Hence, the control of rye B chromosome non-disjunction is also active in sporophytic cells.

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Abbreviations

CT:

Chromosome territory

Cen:

Centromere

FISH:

Fluorescence in situ hybridization

NOR:

Nucleolar organizing region

RSD:

Random spatial distribution

References

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

    Article  PubMed  CAS  Google Scholar 

  • Acosta MC, Moscone EA (2011) B chromosomes in Nierembergia aristata (Solanaceae): nucleolar activity and competition with the A chromosomes. Cytogenet Genome Res 132:105–112

    Article  PubMed  CAS  Google Scholar 

  • Ambros P, Schweizer D (1976) The Giemsa C-banded karyotype of Arabidopsis thaliana (L.) Heynh. Arabidopsis Inf Serv 13:167–171

    Google Scholar 

  • Aragon-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  CAS  Google Scholar 

  • Baker M (2011) Long noncoding RNAs: the search for function. Nat Methods 8:379–383

    Article  CAS  Google Scholar 

  • Bancaud A, Huet S, Daigle N, Mozziconacci J, Beaudouin J, Ellenberg J (2009) Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. EMBO J 28:3785–3798

    Article  PubMed  CAS  Google Scholar 

  • Barow M, Meister A (2003) Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size. Plant Cell Environ 26:571–584

    Article  Google Scholar 

  • Berchtold D, Fesser S, Bachmann G, Kaiser A, Eilert JC, Frohns F, Sadoni N, Muck J, Kremmer E, Eick D, Layer PG, Zink D (2011) Nuclei of chicken neurons in tissues and three-dimensional cell cultures are organized into distinct radial zones. Chromosome Res 19:165–182

    Article  PubMed  CAS  Google Scholar 

  • Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, Allshire RC (2001) Requirement of heterochromatin for cohesion at centromeres. Science 294:2539–2542

    Article  PubMed  CAS  Google Scholar 

  • Berr A, Schubert I (2007) Interphase chromosome arrangement in Arabidopsis thaliana is similar in differentiated and meristematic tissues and shows a transient mirror symmetry after nuclear division. Genetics 176:853–863

    Article  PubMed  Google Scholar 

  • Berr A, Pecinka A, Meister A, Kreth G, Fuchs J, Blattner FR, Lysak MA, Schubert I (2006) Chromosome arrangement and nuclear architecture but not centromeric sequences are conserved between Arabidopsis thaliana and Arabidopsis lyrata. Plant J 48:771–783

    Article  PubMed  CAS  Google Scholar 

  • Blat Y, Kleckner N (1999) Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region. Cell 98:249–259

    Article  PubMed  CAS  Google Scholar 

  • Blunden R, Wilkes TJ, Forster JW, Jimenez MM, Sandery MJ, Karp A, Jones RN (1993) Identification of the E3900 family, a 2nd family of rye chromosome-B specific repeated sequences. Genome 36:706–711

    Article  PubMed  CAS  Google Scholar 

  • Bouzinba-Segard H, Guais A, Francastel C (2006) Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc Natl Acad Sci USA 103:8709–8714

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Camacho JPM, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution. Philos Trans R Soc Lond B Biol Sci 355:163–178

    Article  PubMed  CAS  Google Scholar 

  • Carchilan M, Delgado M, Ribeiro T, Costa-Nunes P, Caperta A, Morais-Cecilio L, Jones RN, Viegas W, Houben A (2007) Transcriptionally active heterochromatin in rye B chromosomes. Plant Cell 19:1738–1749

    Article  PubMed  CAS  Google Scholar 

  • Carchilan M, Kumke K, Mikolajewski S, Houben A (2009) Rye B chromosomes are weakly transcribed and might alter the transcriptional activity of A chromosome sequences. Chromosoma 118:607–616

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Chiavarino AM, Rosato M, Manzanero S, Jimenez G, Gonzalez-Sanchez M, Puertas MJ (2000) Chromosome nondisjunction and instabilities in tapetal cells are affected by B chromosomes in maize. Genetics 155:889–897

    PubMed  CAS  Google Scholar 

  • Cremer T, Cremer M (2010) Chromosome territories. Cold Spring Harb Perspect Biol 2:a003889

    Article  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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Delgado M, Morais-Cecilio L, Neves N, Jones RN, Viegas W (1995) The influence of B chromosomes on rDNA organization in rye interphase nuclei. Chromosome Res 3:487–491

    Article  PubMed  CAS  Google Scholar 

  • Delgado M, Caperta A, Ribeiro T, Viegas W, Jones RN, Morais-Cecilio L (2004) Different numbers of rye B chromosomes induce identical compaction changes in distinct A chromosome domains. Cytogenet Genome Res 106:320–324

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Endo TR, Nasuda S, Jones N, Dou Q, Akahori A, Wakimoto M, Tanaka H, Niwa K, Tsujimoto H (2008) Dissection of rye B chromosomes, and nondisjunction properties of the dissected segments in a common wheat background. Genes Genet Syst 83:23–30

    Article  PubMed  Google Scholar 

  • Francki MG (2001) Identification of Bilby, a diverged centromeric Ty1-copia retrotransposon family from cereal rye (Secale cereale L.). Genome 44:266–274

    PubMed  CAS  Google Scholar 

  • Fransz P, De Jong JH, Lysak M, Castiglione MR, 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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Gill BS, Kimber G (1974) The Giemsa C-banded karyotype of rye. Proc Natl Acad Sci USA 71:1247–1249

    Article  PubMed  CAS  Google Scholar 

  • Göndör A, Ohlsson R (2009) Chromosome crosstalk in three dimensions. Nature 461:212–217

    Article  PubMed  Google Scholar 

  • Guacci V, Hogan E, Koshland D (1994) Chromosome condensation and sister chromatid pairing in budding yeast. J Cell Biol 125:517–530

    Article  PubMed  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Houben A, Kynast RG, Heim U, Hermann H, Jones RN, Forster JW (1996) Molecular cytogenetic characterisation of the terminal heterochromatic segment of the B-chromosome of rye (Secale cereale). Chromosoma 105:97–103

    Article  PubMed  CAS  Google Scholar 

  • Houben A, Orford SJ, Timmis JN (2006) In situ hybridization to plant tissues and chromosomes. Methods Mol Biol 326:203–218

    PubMed  CAS  Google Scholar 

  • Jones RN (1991) B-chromosome drive. Am Nat 137:430–442

    Article  Google Scholar 

  • Jones N, Houben A (2003) B chromosomes in plants: escapees from the A chromosome genome? Trends Plant Sci 8:417–423

    Article  PubMed  CAS  Google Scholar 

  • Jones RN, Rees H (1982) B chromosomes, 1st edn. Academic, London

    Google Scholar 

  • Lanctôt C, Cheutin T, Cremer M, Cavalli G, Cremer T (2007) Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nat Rev Genet 8:104–115

    Article  PubMed  Google Scholar 

  • Leach CR, Houben A, Field B, Pistrick K, Demidov D, Timmis JN (2005) Molecular evidence for transcription of genes on a B chromosome in Crepis capillaris. Genetics 171:269–278

    Article  PubMed  CAS  Google Scholar 

  • Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–293

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Masonbrink RE, Birchler JA (2010) Sporophytic nondisjunction of the maize B chromosome at high copy numbers. J Genet Genomics 37:79–84

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • McNally JG, Mazza D (2010) Fractal geometry in the nucleus. EMBO J 29:2–3

    Article  PubMed  CAS  Google Scholar 

  • Metz C (1916) Chromosome studies on the Diptera: II. The paired association of chromosomes in the Diptera and its significance. J Exp Zool 21:213–279

    Article  Google Scholar 

  • Misteli T, Soutoglou E (2009) The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat Rev Mol Cell Biol 10:243–254

    Article  PubMed  CAS  Google Scholar 

  • Morais-Cecilio L, Delgado M, Jones RN, Viegas W (1996) Painting rye B chromosomes in wheat: interphase chromatin organization, nuclear disposition and association in plants with two, three or four Bs. Chromosome Res 4:195–200

    Article  PubMed  CAS  Google Scholar 

  • Morais-Cecilio L, Delgado M, Jones RN, Viegas W (2000) Modification of wheat rDNA loci by rye B chromosomes: a chromatin organization model. Chromosome Res 8:341–351

    Article  PubMed  CAS  Google Scholar 

  • Müntzing A (1948) Cytological studies of extra fragment chromosomes in rye. V. A new fragment type arisen by deletion. Hereditas 34:435–442

    Article  Google Scholar 

  • Müntzing A (1970) Chromosomal variation in the Lindström strain of wheat carrying accessory chromosomes in rye. Hereditas 66:279–286

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Nasmyth K (2005) How do so few control so many? Cell 120:739–746

    Article  PubMed  CAS  Google Scholar 

  • Niwa K, Horiuchi G, Hirai Y (1997) Production and characterization of common wheat with B chromosomes of rye from Korea. Hereditas 126:139–146

    Article  Google Scholar 

  • Pecinka A, Schubert V, Meister A, Kreth G, Klatte M, Lysak MA, Fuchs J, Schubert I (2004) Chromosome territory arrangement and homologous pairing in nuclei of Arabidopsis thaliana are predominantly random except for NOR-bearing chromosomes. Chromosoma 113:258–269

    Article  PubMed  CAS  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. Morph Jb 10:214–330

    Google Scholar 

  • Riley R, Chapman V (1958) The production and phenotypes of wheat-rye chromosome addition lines. Heredity 12:301–315

    Article  Google Scholar 

  • Sandery MJ, Forster JW, Blunden R, Jones RN (1990) Identification of a family of repeated sequences on the rye B-chromosome. Genome 33:908–913

    Article  CAS  Google Scholar 

  • Schubert I, Shaw P (2011) Organization and dynamics of plant interphase chromosomes. Trends Plant Sci 16:273–281

    Article  PubMed  CAS  Google Scholar 

  • Schubert V, Klatte M, Pecinka A, Meister A, Jasencakova Z, Schubert I (2006) Sister chromatids are often incompletely aligned in meristematic and endopolyploid interphase nuclei of Arabidopsis thaliana. Genetics 172:467–475

    Article  PubMed  CAS  Google Scholar 

  • Schubert V, Kim YM, Berr A, Fuchs J, Meister A, Marschner S, Schubert I (2007) Random homologous pairing and incomplete sister chromatid alignment are common in angiosperm interphase nuclei. Mol Genet Genomics 278:167–176

    Article  PubMed  CAS  Google Scholar 

  • Schubert V, Kim YM, Schubert I (2008) Arabidopsis sister chromatids often show complete alignment or separation along a 1.2-Mb euchromatic region but no cohesion “hot spots”. Chromosoma 117:261–266

    Article  PubMed  CAS  Google Scholar 

  • Tomita M, Shinohara K, Morimoto M (2008) Revolver is a new class of transposon-like gene composing the Triticeae genome. DNA Res 15:49–62

    Article  PubMed  CAS  Google Scholar 

  • Vazquez J, Belmont AS, Sedat JW (2002) The dynamics of homologous chromosome pairing during male Drosophila meiosis. Curr Biol 12:1473–1483

    Article  PubMed  CAS  Google Scholar 

  • Volpe T, Schramke V, Hamilton GL, White SA, Teng G, Martienssen RA, Allshire RC (2003) RNA interference is required for normal centromere function in fission yeast. Chromosome Res 11:137–146

    Article  PubMed  CAS  Google Scholar 

  • Volpi EV, Sheer D, Uhlmann F (2001) Cohesion, but not too close. Curr Biol 11:R378

    Article  PubMed  CAS  Google Scholar 

  • Wilkes TM, Francki MG, Langridge P, Karp A, Jones RN, Forster JW (1995) Analysis of rye B-chromosome structure using fluorescence in situ hybridization (FISH). Chromosome Res 3:466–472

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Steve Reader for providing seeds, Katrin Kumke for excellent technical assistance, Jörg Fuchs for sorting of nuclei and Ingo Schubert for critical reading of the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft (HO 1779/10-1).

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Authors and Affiliations

  1. Leibniz Institute of Plant Genetics and Crop Plant Research, 06466, Gatersleben, Germany

    Veit Schubert, Armin Meister & Andreas Houben

  2. Arid Land Research Center, Tottori University, 1390 Hamasaka, Tottori, 680-0001, Japan

    Hisashi Tsujimoto

  3. Graduate School of Agriculture, Kyoto University, Kyoto, 6006-8502, Japan

    Takashi Ryu Endo

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  1. Veit Schubert
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  2. Armin Meister
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  3. Hisashi Tsujimoto
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  4. Takashi Ryu Endo
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Correspondence to Veit Schubert.

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Responsible Editor: Conly Rieder.

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Supplementary Table 1

Dimensions and areas of nuclei (blue), chromosome territories (CTs, red) and centromere (Cen, green) signals (mean values per addition line and ploidy level) used for the RSD computer model simulations (DOC 61 kb)

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Schubert, V., Meister, A., Tsujimoto, H. et al. Similar rye A and B chromosome organization in meristematic and differentiated interphase nuclei. Chromosome Res 19, 645–655 (2011). https://doi.org/10.1007/s10577-011-9224-5

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