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Composition and formation of heterochromatin in Arabidopsis thaliana

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Abstract

The term heterochromatin has been applied to both large-scale, microscopically visible chromocentres and small-scale, silent genes located outside chromocentres. This may cause confusion in the interpretation of epigenetic marks for both features. The model plant Arabidopsis thaliana provides an excellent system to investigate composition and function of chromatin states at different levels of organization. In this review we will discuss recent developments in molecular networks underlying gene silencing and the relationship with visible heterochromatin in Arabidopsis.

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References

  • Aufsatz W, Mette MF, van der Winden J, Matzke M, Matzke AJM (2002) HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J 21: 6832–6841.

    Article  CAS  PubMed  Google Scholar 

  • Aufsatz W, Mette M, Matzke A, Matzke M (2004) The role of MET1 in RNA-directed de-novo and maintenance methylation of CG dinucleotides. Plant Mol Biol 54: 793–804.

    Article  CAS  PubMed  Google Scholar 

  • Bao N, Lye KW, Barton MK (2004) MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev Cell 7: 653–662.

    Article  CAS  PubMed  Google Scholar 

  • Baumbusch LO, Thorstensen T, Krauss V et al. (2001). The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucl. Acids Res 29: 4319–4333.

    Article  CAS  PubMed  Google Scholar 

  • Brzeski J, Jerzmanowski A (2004) Plant chromatin–epigenetics linked to ATP-dependent remodeling and architectural proteins. FEBS Lett 567: 15–19.

    Article  CAS  PubMed  Google Scholar 

  • Chan SW-L, Zilberman D, Xie Z, Johansen LK, Carrington JC, Jacobsen SE (2004) RNA silencing genes control de novo DNA methylation. Science 303: 1336.

    CAS  PubMed  Google Scholar 

  • Finnegan EJ, Peacock WJ, Dennis ES (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc Natl Acad Sci USA 93: 8449–8454.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fransz P, Soppe W, Schubert I (2003) Heterochromatin in interphase nuclei of Arabidopsis thaliana. Chromosome Res 11: 227–240.

    Article  CAS  PubMed  Google Scholar 

  • Gaudin V, Libault M, Pouteau S et al. (2001). Mutations in LIKE HETEROCHROMATIN PROTEIN 1 affect flowering time and plant architecture in Arabidopsis. Development 128: 4847–4858.

    CAS  PubMed  Google Scholar 

  • Gendrel AV, Lippman Z, Yordan C, Colot V, Martienssen RA (2002) Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297: 1871–1873.

    Article  CAS  PubMed  Google Scholar 

  • Hennig L, Taranto P, Walser M, Schonrock N, Gruissem W (2003) Arabidopsis MSI1 is required for epigenetic maintenance of reproductive development. Development 130: 2555–2565.

    Article  CAS  PubMed  Google Scholar 

  • Herr AJ, Jensen MB, Dalmay T, Baulcombe DC (2005) RNA polymerase IV directs silencing of endogenous DNA. Science 308: 118–120.

    Article  CAS  PubMed  Google Scholar 

  • Iida T, Suetake I, Tajima S et al. (2002) PCNA clamp facilitates action of DNA cytosine methyltransferase 1 on hemimethylated DNA. Genes Cells 7: 997–1007.

    CAS  PubMed  Google Scholar 

  • Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556–560.

    Article  CAS  PubMed  Google Scholar 

  • Jackson J, Johnson L, Jasencakova Z et al. (2004) Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112: 308–315.

    Article  CAS  PubMed  Google Scholar 

  • Jasencakova Z, Soppe WJ, Meister A, Gernand D, Turner BM, Schubert I (2003) Histone modifications in Arabidopsis – high methylation of H3 lysine 9 is dispensable for constitutive heterochromatin. Plant J 33: 471–480.

    Article  CAS  PubMed  Google Scholar 

  • Johnson L, Cao X, Jacobsen S (2002) Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12: 1360–1367.

    CAS  PubMed  Google Scholar 

  • Kakutani T, Munakata, K., Richards EJ, Hirochika H (1999) Meiotically and mitotically stable inheritance of DNA hypomethylation induced by ddm1 mutation of Arabidopsis thaliana. Genetics 151: 831–838.

    CAS  PubMed  Google Scholar 

  • Kanno T, Mette MF, Kreil DP, Aufsatz W, Matzke M, Matzke AJM (2004). Involvement of putative SNF2 chromatin remodeling protein DRD1 in RNA-directed DNA methylation. Curr Biol 14: 801–805.

    Article  CAS  PubMed  Google Scholar 

  • Kanno T, Aufsatz W, Jaligot E, Mette MF, Matzke M, Matzke AJ (2005a). A SNF2-like protein facilitates dynamic control of DNA methylation. EMBO Rep 6: 649–655.

    Article  CAS  PubMed  Google Scholar 

  • Kanno T, Huettel B, Mette MF et al. (2005b) Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet 37: 761–765.

    Google Scholar 

  • Kaya H, Shibahara KI, Taoka, KI, Iwabuchi M, Stillman B, Araki T (2001). FASCIATA genes for chromatin assembly factor-1 in arabidopsis maintain the cellular organization of apical meristems. Cell 104: 131–142.

    Article  CAS  PubMed  Google Scholar 

  • Klochendler-Yeivin A, Muchardt C, Yaniv M (2002) SWI/SNF chromatin remodeling and cancer. Curr Opin Genet Dev 12: 73–79.

    Article  CAS  PubMed  Google Scholar 

  • Lachner M, O'Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116–120.

    Article  CAS  PubMed  Google Scholar 

  • Lehnertz B, Ueda Y, Derijck AAHA et al. (2003) Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 13: 1192–1200.

    Article  CAS  PubMed  Google Scholar 

  • Libault M, Tessadori F, Germann S, Snijder B, Fransz P, Gaudin V (2005). The Arabidopsis LHP1 protein is a component of euchromatin. Planta DOI: 10.1007/s00425-005-0129-4.

  • Lindroth AM, Shultis D, Jasencakova Z et al. (2004). Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J 23: 4286–4296.

    Article  CAS  PubMed  Google Scholar 

  • Lippman Z, Gendrel AV, Black M et al. (2004). Role of transposable elements in heterochromatin and epigenetic control. Nature 430: 471–476.

    Article  CAS  PubMed  Google Scholar 

  • Liu J, He Y, Amasino R, Chen X (2004) siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes Dev 18: 2873–2878.

    CAS  PubMed  Google Scholar 

  • Malagnac F, Bartee L, Bender J (2002) An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J 21: 6842–6852.

    Article  CAS  PubMed  Google Scholar 

  • Mathieu O, Probst AV, Paszkowski J (2005) Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis. EMBO J 24: 2783–2791.

    Article  CAS  PubMed  Google Scholar 

  • Melquist S, Bender J (2004) An internal rearrangement in an Arabidopsis inverted repeat locus impairs DNA methylation triggered by the locus. Genetics 166: 437–448.

    Article  CAS  PubMed  Google Scholar 

  • Mittelsten Scheid O, Probst AV, Afsar K, Paszkowski J (2002) Two regulatory levels of transcriptional gene silencing in Arabidopsis. Proc Natl Acad Sci USA 99: 13659–13662.

    PubMed  Google Scholar 

  • Nakahigashi K, Jasencakova Z, Schubert I, Goto K (2005) The Arabidopsis HETEROCHROMATIN PROTEIN1 homolog (TERMINAL FLOWER2) silences genes within euchromatic region but not genes positioned in heterochromatin. Plant Cell Physiol DOI: 10.1093/pcp/pci195.7

  • Naumann K, Fischer A, Hofmann I et al. (2005) Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis. EMBO J 24 1418–1429.

    Article  CAS  PubMed  Google Scholar 

  • Onodera Y, Haag JR, Ream T, Nunes PC, Pontes O, Pikaard CS (2005) Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120: 613–622.

    Article  CAS  PubMed  Google Scholar 

  • Peters AH, Kubicek S, Mechtler K et al. (2003) Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 12, 1577–1589.

    Article  CAS  PubMed  Google Scholar 

  • Probst AV, Fransz PF, Paszkowski J, Mittelsten Scheid O (2003) Two means of transcriptional reactivation within heterochromatin. Plant J 33: 743–749.

    Article  CAS  PubMed  Google Scholar 

  • Probst AV, Fagard M, Proux F et al. (2004) Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16: 1021–1034.

    Article  CAS  PubMed  Google Scholar 

  • Quivy JP, Roche D, Kirschner D, Tagami H, Nakatani Y, Almouzni G (2004) A CAF-1 dependent pool of HP1 during heterochromatin duplication. EMBO J 23: 3516–3526.

    Article  CAS  PubMed  Google Scholar 

  • Ramsahoye BH, Biniszkiewicz D, Lyko F, Clark V, Bird AP, Jaenisch R (2000) Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. PNAS 97: 5237–5242.

    Article  CAS  PubMed  Google Scholar 

  • Rangwala SH, Richards EJ (2004) The value-added genome: building and maintaining genomic cytosine methylation landscapes. Curr Opin Genet Dev 14: 686–691.

    Article  CAS  PubMed  Google Scholar 

  • Schotta G, Lachner M, Sarma K et al. (2004) A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 18: 1251–1262.

    Article  CAS  PubMed  Google Scholar 

  • Soppe WJJ, Jacobsen SE, Alonso-Blanco C et al. (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.

    Article  CAS  PubMed  Google Scholar 

  • Soppe WJ, Jasencakova Z, Houben A et al. (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21: 6549–6559.

    Article  CAS  PubMed  Google Scholar 

  • Takeda S, Tadele Z, Hofmann I et al. (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 

  • Tamaru H, Selker EU (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. 414: 277– 283.

  • Tariq M, Saze H, Probst AV, Lichota J Habu Y, Paszkowski J (2003) Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci USA 100: 8823–8827.

    Article  CAS  PubMed  Google Scholar 

  • Tessadori F, van Driel R, Fransz P (2004) Cytogenetics as a tool to study gene regulation. Trends Plant Sci 9: 147–153.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Vaucheret H (2005) MicroRNA-dependent trans-acting siRNA production. Sci STKE 2005: pe43.

  • Xie Z, Johansen LK, Gustafson AM et al. (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biology 2: e104.

    Google Scholar 

  • Zemach A, Li Y, Wayburn B et al. (2005) DDM1 binds Arabidopsis methyl-CpG binding domain proteins and affects their subnuclear localization. Plant Cell 17: 1549–1558.

    Article  CAS  PubMed  Google Scholar 

  • Zilberman D, Cao X, Jacobsen SE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716–719.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Swammerdam Institute for Life Sciences, BioCentrum Amsterdam, University of Amsterdam, Kruislaan 318, 1098 SM, Amsterdam, The Netherlands

    P. Fransz, R. ten Hoopen & F. Tessadori

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  1. P. Fransz
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  2. R. ten Hoopen
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  3. F. Tessadori
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Correspondence to P. Fransz.

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Fransz, P., ten Hoopen, R. & Tessadori, F. Composition and formation of heterochromatin in Arabidopsis thaliana. Chromosome Res 14, 71–82 (2006). https://doi.org/10.1007/s10577-005-1022-5

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