Skip to main content
Log in

BRU1 Maintains Configuration of the Euchromatic Subchromosomal Domain in the Nucleus of Arabidopsis

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Chromatin states are inseparably associated with regulation of genes. In yeast and animals, chromatin states also correlate with the configuration and spatial localization pattern of chromosomal domains in the nucleus. In plants, however, the dynamics of such domains associated with gene regulation is poorly understood except for heterochromatic domains. We have previously reported several euchromatic regions of Arabidopsis chromosomes where genes are preferentially upregulated by a defect in BRU1—a nuclear factor involved in DNA damage responses and epigenetic gene regulation. In this study, we present a cytogenetic characterization of one of these subchromosomal regions, SCR1. In nuclei of wild-type leaf cells, the 174-kb SCR1 region was moderately condensed near nucleolus organizing region 4 (NOR4). In bru1 mutants, the confined localization pattern of SCR1 was stochastically disrupted. In contrast, bru1 defects did not affect the localization patterns of NOR4 and another 149-kb euchromatic region in which gene activity was not altered in bru1. The degree of confinement of SCR1 in the nucleus varied between leaves, hypocotyls, and undifferentiated calli, but not drastically. These results suggest that BRU1 plays a role in maintaining the configuration of a euchromatic subchromosomal domain that is a potential determinant in the control of gene activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3a,b
Fig. 4a,b
Fig. 5
Fig. 6a,b

Similar content being viewed by others

References

  • Andrulis ED, Zappulla DC, Ansari A, Perrod S, Laiosa CV, Gartenberg MR, Sternglanz R (2002) Esc1, a nuclear periphery protein required for Sir4-based plasmid anchoring and partitioning. Mol Cell Biol 22:8292–8301

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV, Tariq M, Paszkowski J (2004) Chromatin techniques for plant cells. Plant J 39:776–789

    Article  CAS  PubMed  Google Scholar 

  • Carmen AA, Milne L, Grunstein M (2002) Acetylation of the yeast histone H4 N terminus regulates its binding to heterochromatin protein SIR3. J Biol Chem 277:4778–4781

    Article  CAS  PubMed  Google Scholar 

  • Carvalho A, Polanco C, Lima-Brito J, Guedes-Pinto H (2010) Differential rRNA genes expression in hexaploid wheat related to NOR methylation. Plant Mol Biol Rep 28:403–412

    Article  CAS  Google Scholar 

  • Copenhaver GP, Nickel K, Kuromori T, Benito MI, Kaul S, Lin X, Bevan M, Murphy G, Harris B, Parnell LD, McCombie WR, Martienssen RA, Marra M, Preuss D (1999) Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286:2468–2474

    Article  CAS  PubMed  Google Scholar 

  • Duro E, Lundin C, Ask K, Sanchez-Pulido L, MacArtney TJ, Toth R, Ponting CP, Groth A, Helleday T, Rouse J (2010) Identification of the MMS22L-TONSL complex that promotes homologous recombination. Mol Cell 40:632–644

    Article  CAS  PubMed  Google Scholar 

  • Fang Y, Spector DL (2005) Centromere positioning and dynamics in living Arabidopsis plants. Mol Biol Cell 16:5710–5718

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Finlan LE, Sproul D, Thomson I, Boyle S, Kerr E, Perry P, Ylstra B, Chubb JR, Bickmore WA (2008) Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet 4:e1000039

    Article  PubMed Central  PubMed  Google Scholar 

  • Fransz P, De JJH, 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  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, van Steensel B (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453:948–951

    Article  CAS  PubMed  Google Scholar 

  • Guyomarc’h S, Vernoux T, Traas J, Zhou DX, Delarue M (2004) MGOUN3, an Arabidopsis gene with TetratricoPeptide-Repeat-related motifs, regulates meristem cellular organization. J Exp Bot 55:673–684

    Article  PubMed  Google Scholar 

  • Guyomarc’h S, Benhamed M, Lemonnier G, Renou JP, Zhou DX, Delarue M (2006) MGOUN3: evidence for chromatin-mediated regulation of FLC expression. J Exp Bot 57:2111–2119

    Article  PubMed  Google Scholar 

  • Haber JE (1999) Sir-Ku-itous routes to make ends meet. Cell 97:829–832

    Article  CAS  PubMed  Google Scholar 

  • Hecht A, Laroche T, Strahl-Bolsinger S, Gasser SM, Grunstein M (1995) Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell 80:583–592

    Article  CAS  PubMed  Google Scholar 

  • Kanno T, Yoshikawa M, Habu Y (2013) Locus-specific requirements of DDR complexes for gene-body methylation of TAS genes in Arabidopsis thaliana. Plant Mol Biol Rep. doi:10.1007/s11105-012-0554-z

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Li G, Reinberg D (2011) Chromatin higher-order structures and gene regulation. Curr Opin Genet Dev 21:175–186

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Meaburn KJ, Misteli T (2007) Cell biology: chromosome territories. Nature 445:379–781

    Article  CAS  PubMed  Google Scholar 

  • Meister P, Towbin BD, Pike BL, Ponti A, Gasser SM (2010) The spatial dynamics of tissue-specific promoters during C. elegans development. Genes Dev 24:766–782

    Article  CAS  PubMed  Google Scholar 

  • Neméth A, Langst G (2011) Genome organization in and around the nucleolus. Trends Genet 27:149–156

    Article  PubMed  Google Scholar 

  • O’Connell BC, Adamson B, Lydeard JR, Sowa ME, Ciccia A, Bredemeyer AL, Schlabach M, Gygi SP, Elledge SJ, Harper JW (2010) A genome-wide camptothecin sensitivity screen identifies a mammalian MMS22L-NFKBIL2 complex required for genomic stability. Mol Cell 40:645–657

    Article  PubMed Central  PubMed  Google Scholar 

  • O’Donnell L, Panier S, Wildenhain J, Tkach JM, Al-Hakim A, Landry MC, Escribano-Diaz C, Szilard RK, Young JT, Munro M, Canny MD, Kolas NK, Zhang W, Harding SM, Ylanko J, Mendez M, Mullin M, Sun T, Habermann B, Datti A, Bristow RG, Gingras AC, Tyers MD, Brown GW, Durocher D (2010) The MMS22L-TONSL complex mediates recovery from replication stress and homologous recombination. Mol Cell 40:619–631

    Article  PubMed Central  PubMed  Google Scholar 

  • Ohno Y, Narangajavana J, Yamamoto A, Hattori T, Kagaya Y, Paszkowski J, Gruissem W, Hennig L, Takeda S (2011) Ectopic gene expression and organogenesis in Arabidopsis mutants missing BRU1 required for genome maintenance. Genetics 189:83–95

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SW, Solovei I, Brugman W, Gräf S, Flicek P, Kerkhoven RM, van Lohuizen M, Reinders M, Wessels L, van Steensel B (2010) Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell 38:603–613

    Article  CAS  PubMed  Google Scholar 

  • Piwko W, Olma MH, Held M, Bianco JN, Pedrioli PG, Hofmann K, Pasero P, Gerlich DW, Peter M (2010) RNAi-based screening identifies the Mms22L-Nfkbil2 complex as a novel regulator of DNA replication in human cells. EMBO J 29:4210–4222

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schubert V, Berr A, Meister A (2012) Interphase chromatin organisation in Arabidopsis nuclei: constraints versus randomness. Chromosoma 121:369–387

    Article  CAS  PubMed  Google Scholar 

  • Simon JA, Kingston RE (2009) Mechanisms of polycomb gene silencing: knowns and unknowns. Nat Rev Mol Cell Biol 10:697–708

    CAS  PubMed  Google Scholar 

  • Solovei I, Kreysing M, Lanctot C, Kösem S, Peichl L, Cremer T, Guck J, Joffe B (2009) Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137:356–368

    Article  CAS  PubMed  Google Scholar 

  • Soppe WJ, Jasencakova Z, Houben A, Kakutani T, Meister A, Huang MS, Jacobsen SE, Schubert I, Fransz PF (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21:6549–6559

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Inagaki S, Nakajima S, Akashi T, Ohto MA, Kobayashi M, Seki M, Shinozaki K, Kato T, Tabata S, Nakamura K, Morikami A (2004) A novel Arabidopsis gene TONSOKU is required for proper cell arrangement in root and shoot apical meristems. Plant J 38:673–684

    Article  CAS  PubMed  Google Scholar 

  • Taddei A, Hediger F, Neumann FR, Gasser SM (2004) The function of nuclear architecture: a genetic approach. Annu Rev Genet 38:305–345

    Article  CAS  PubMed  Google Scholar 

  • Taddei A, Van Houwe G, Nagai S, Erb I, van Nimwegen E, Gasser SM (2009) The functional importance of telomere clustering: global changes in gene expression result from SIR factor dispersion. Genome Res 19:611–625

    Article  CAS  PubMed  Google Scholar 

  • Takeda S, Tadele Z, Hofmann I, Probst AV, Angelis KJ, Kaya H, Araki T, Mengiste T, Mittelsten SO, Shibahara K, Scheel D, Paszkowski J (2004) BRU1, a novel link between responses to DNA damage and epigenetic gene silencing in Arabidopsis. Genes Dev 18:782–793

    Article  CAS  PubMed  Google Scholar 

  • Takizawa T, Gudla PR, Guo L, Lockett S, Misteli T (2008) Allele-specific nuclear positioning of the monoallelically expressed astrocyte marker GFAP. Genes Dev 22:489–498

    Article  CAS  PubMed  Google Scholar 

  • Tiang CL, He Y, Pawlowski WP (2012) Chromosome organization and dynamics during interphase, mitosis, and meiosis in plants. Plant Physiol 158:26–34

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Towbin BD, Meister P, Gasser SM (2009) The nuclear envelope—a scaffold for silencing? Curr Opin Genet Dev 19:180–186

    Article  CAS  PubMed  Google Scholar 

  • Vongs A, Kakutani T, Martienssen RA, Richards EJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260:1926–1928

    Article  CAS  PubMed  Google Scholar 

  • Williams RR, Azuara V, Perry P, Sauer S, Dvorkina M, Jørgensen H, Roix J, McQueen P, Misteli T, Merkenschlager M, Fisher AG (2006) Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J Cell Sci 119:132–140

    Article  CAS  PubMed  Google Scholar 

  • Zullo JM, Demarco IA, Piqué-Regi R, Gaffney DJ, Epstein CB, Spooner CJ, Luperchio TR, Bernstein BE, Pritchard JK, Reddy KL, Singh H (2012) DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell 149:1474–1487

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Koichi Watanabe for advices for FISH analysis, and Chiharu Ueguchi, Ken-ichi Kurotani and Yosuke Toda for helpful comments. This work was in part supported by KAKENHI 23012019.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shin Takeda.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 104 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ohno, Y., Nishimura, T., Hattori, T. et al. BRU1 Maintains Configuration of the Euchromatic Subchromosomal Domain in the Nucleus of Arabidopsis. Plant Mol Biol Rep 32, 19–27 (2014). https://doi.org/10.1007/s11105-013-0596-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-013-0596-x

Keywords

Navigation