Skip to main content

Epigenetic Characterization of Satellite DNA in Sugar Beet (Beta vulgaris)

  • Chapter
  • First Online:

Part of the book series: RNA Technologies ((RNATECHN))

Abstract

Satellite DNA is a major and abundant component of plant genomes and comprises important genomic regions such as heterochromatic knobs and centromeric chromatin. However, technical barriers of assembling first- and second-generation sequencing data hampered the complete arrangement of satellite DNAs in current plant genome sequences. Consequently, heterochromatic and centromeric regions possessing satellite DNA lack detailed characterization and assignment, which limits knowledge about their epigenetic status. We applied methods to overcome these limitations and to gain insight into the epigenetic modifications of satellite DNA-rich heterochromatic and centromeric regions of the sugar beet (Beta vulgaris) genome. Sugar beet is an important crop of temperate climate zones, which provides nearly 30% of the world’s annual sugar needs. Due to the 11% of the genome consisting of satellite DNAs, sugar beet is a suitable research object for comparative investigation and epigenetic characterization of this repeat class. We analyzed the epigenetic modifications of satellite DNA by using bisulfite sequencing, chromatin immunoprecipitation followed by sequencing (ChiP-Seq) using antibodies against histone CenH3 and dimethylated H3K9me2, and small RNA-seq data. Immunostaining of methylated cytosines and histone modifications combined with fluorescent in situ hybridization (FISH) coupled with super-resolution fluorescence microscopy complemented the epigenetic analysis. As a result, we uncovered individual epigenetic characteristics of plant satellite DNAs at high resolution and hypothesized a model for satellite DNA-directed heterochromatization.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Allshire RC, Karpen GH (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet 9:923–937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Bio Report 9:186–198

    Article  Google Scholar 

  • Carroll CW, Straight AF (2006) Centromere formation: from epigenetics to self-assembly. Trends Cell Biol 16:70–78

    Article  CAS  PubMed  Google Scholar 

  • Chan SW, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6:351–360

    Article  CAS  PubMed  Google Scholar 

  • De Bock TSM (1986) The genus Beta: domestication, tayonomy and interspecific hybridization for plant breeding. Acta Hortic 82:335–344

    Article  Google Scholar 

  • Demidov D, Schubert V, Kumke K et al. (2014) Anti-phosphorylated histone H2AThr120: a universal microscopic marker for centromeric chromatin of mono- and holocentric plant species. Cytogenet Genome Res 143:150–156

    Article  CAS  PubMed  Google Scholar 

  • Dohm JC, Minoche AE, Holtgräwe D et al. (2014) The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 505:546–549

    Article  CAS  PubMed  Google Scholar 

  • Dong Q, Han F (2012) Phosphorylation of histone H2A is associated with centromere function and maintenance in meiosis. Plant J 71:800–809

    Article  CAS  PubMed  Google Scholar 

  • Fischer HE (1989) Origin of the Weiße Schlesische Rübe (white Silesian beet) and resynthesis of sugar beet. Euphytica 41:75–80

    Article  Google Scholar 

  • Flavell RB, Bennett MD, Smith JB et al. (1974) Genome size and proportion of repeated nucleotide-sequence DNA in plants. Biochem Genet 12:257–269

    Article  CAS  PubMed  Google Scholar 

  • Ford-Lloyd BV, Williams JT (1975) A revision of Beta section Vulgares (Chenopodiaceae), with new light on the origin of cultivated beets. Bot J Linn Soc 71:89–102

    Article  Google Scholar 

  • Fuchs J, Demidov D, Houben A et al. (2006) Chromosomal histone modification patterns—from conservation to diversity. Trends Plant Sci 11:199–208

    Article  CAS  PubMed  Google Scholar 

  • Gent JI, Madzima TF, Bader R et al. (2014) Accessible DNA and relative depletion of H3K9me2 at maize loci undergoing RNA-directed DNA methylation. Plant Cell 26:903–917

    Article  Google Scholar 

  • Ghildiyal M, Zamore PD (2009) Small silencing RNAs: an expanding universe. Nat Rev Genet 10:94–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hemleben V, Kovarik A, Torres-Ruiz RA et al. (2007) Plant highly repeated satellite DNA: molecular evolution, distribution and use for identification of hybrids. Syst Biodivers 5:277–289

    Article  Google Scholar 

  • Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447:418–424

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Heun P, Erhardt S, Blower MD et al. (2006) Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev Cell 10:303–315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howman EV, Fowler KJ, Newson AJ et al (2000) Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc Natl Acad Sci U S A 97:1148–1153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Johnson LM, Bostick M, Zhang X et al. (2007) The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol 17:379–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13:484–492

    Article  CAS  PubMed  Google Scholar 

  • Kadereit G, Hohmann S, Kadereit JW (2006) A synopsis of Chenopodiaceae subfam. Betoideae and notes on the taxonomy of Beta. Willdenowia 36:9–19

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kim IS, Lee M, Park KC et al. (2012) Roles of Mis18α in epigenetic regulation of centromeric chromatin and CENP-A loading. Mol Cell 46:260–273

    Article  CAS  PubMed  Google Scholar 

  • Koo DH, Han F, Birchler JA et al. (2011) Distinct DNA methylation patterns associated with active and inactive centromeres of the maize B chromosome. Genome Res 21:908–914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kowar T, Zakrzewski F, Macas J et al. (2016) Repeat composition of CenH3-chromatin and H3K9me2-marked heterochromatin in sugar beet (Beta vulgaris). BMC Plant Biol 16:120

    Article  PubMed  PubMed Central  Google Scholar 

  • Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lermontova I, Koroleva O, Rutten T et al. (2011) Knockdown of CENH3 in Arabidopsis reduces mitotic divisions and causes sterility by disturbed meiotic chromosome segregation. Plant J 68:40–50

    Article  CAS  PubMed  Google Scholar 

  • Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Lu F, Cui X et al. (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61:395–420

    Article  CAS  PubMed  Google Scholar 

  • Martienssen RA (2003) Maintenance of heterochromatin by RNA interference of tandem repeats. Nat Genet 35:213–214

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Paesold S, Borchardt D, Schmidt T et al. (2012) A sugar beet (Beta vulgaris L.) reference FISH karyotype for chromosome and chromosome-arm identification, integration of genetic linkage groups and analysis of major repeat family distribution. Plant J 72:600–611

    Article  CAS  PubMed  Google Scholar 

  • Palomeque T, Lorite P (2008) Satellite DNA in insects: a review. Heredity 100:564–573

    Article  CAS  PubMed  Google Scholar 

  • Peng JC, Karpen GH (2008) Epigenetic regulation of heterochromatic DNA stability. Curr Opin Genet Dev 18:204–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pikaard CS, Haag JR, Pontes OMF et al. (2012) A transcription fork model for Pol IV and Pol V-dependent RNA-directed DNA methylation. Cold Spring Harb Symp Quant Bio 77:205–212

    Article  CAS  Google Scholar 

  • Plohl M, Luchetti A, Meštrović N et al. (2008) Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin. Gene 409:72–82

    Article  CAS  PubMed  Google Scholar 

  • Pontier D, Yahubyan G, Vega D et al. (2005) Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev 19:2030–2040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Régnier V, Vagnarelli P, Fukagawa T et al. (2005) CENP-A is required for accurate chromosome segregation and sustained kinetochore association of BubR1. Mol Cell Biol 25:3967–3981

    Article  PubMed  PubMed Central  Google Scholar 

  • Roudier F, Ahmed I, Bérard C et al. (2011) Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30:1928–1938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt T, Heslop-Harrison JS (1998) Genomes, genes and junk: the large-scale organization of plant chromosomes. Trends Plant Sci 3:195–199

    Article  Google Scholar 

  • Schmidt T, Metzlaff M (1991) Cloning and characterization of a beta-vulgaris satellite DNA family. Gene 101:247–250

    Article  CAS  PubMed  Google Scholar 

  • Schmidt T, Jung C, Metzlaff M (1991) Distribution and evolution of two satellite DNAs in the genus Beta. Theor Appl Genet 82:793–799

    Article  CAS  PubMed  Google Scholar 

  • Schmidt M, Hense S, Minoche AE et al. (2014) Cytosine methylation of an ancient satellite family in the wild beet Beta procumbens. Cytogenet Genome Res 143:157–167

    Article  CAS  PubMed  Google Scholar 

  • Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9:465–476

    Article  CAS  PubMed  Google Scholar 

  • Tariq M, Paszkowski J (2004) DNA and histone methylation in plants. Trends Genet 20:244–251

    Article  CAS  PubMed  Google Scholar 

  • Teixeira FK, Colot V (2010) Repeat elements and the Arabidopsis DNA methylation landscape. Heredity 105:14–23

    Article  CAS  PubMed  Google Scholar 

  • Treangen TJ, Salzberg SL (2012) Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet 13:36–46

    CAS  Google Scholar 

  • Ugarkovic D (2005) Functional elements residing within satellite DNAs. EMBO Rep 6:1035–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang G, Ma A, Chow CM et al. (2000) Conservation of heterochromatin protein 1 function. Mol Cell Biol 20:6970–6983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weber B, Schmidt T (2009) Nested Ty3-gypsy retrotransposons of a single Beta procumbens centromere contain a putative chromodomain. Chromosom Res 17:379–396

    Article  CAS  Google Scholar 

  • Weber B, Wenke T, Frömmel U et al. (2010) The Ty1-copia families SALIRE and Cotzilla populating the Beta vulgaris genome show remarkable differences in abundance, chromosomal distribution, and age. Chromosom Res 18:247–263

    Article  CAS  Google Scholar 

  • Weber B, Heitkam T, Holtgräwe D et al. (2013) Highly diverse chromoviruses of Beta vulgaris are classified by chromodomains and chromosomal integration. Mob DNA 4:8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weisshaar B, Himmelbauer H, Schmidt T et al. (2016) Sugar beet BeetMap-3, and steps to improve the genome assembly and genome sequence annotation. W875, Plant & Animal Genome XXIV, San Diego, USA

    Google Scholar 

  • West PT, Li Q, Ji L et al. (2014) Genomic distribution of H3K9me2 and DNA methylation in a maize genome. PLoS One 9:e105267

    Article  PubMed  PubMed Central  Google Scholar 

  • Wollrab C, Heitkam T, Holtgräwe D et al. (2012) Evolutionary reshuffling in the Errantivirus lineage Elbe within the Beta vulgaris genome. Plant J 72:636–651

    Article  CAS  PubMed  Google Scholar 

  • Xu C, Tian J, Mo B (2013) siRNA-mediated DNA methylation and H3K9 dimethylation in plants. Protein &Cell 4:656–663

    Article  CAS  Google Scholar 

  • Yan H, Kikuchi S, Neumann P et al. (2010) Genome-wide mapping of cytosine methylation revealed dynamic DNA methylation patterns associated with genes and centromeres in rice. Plant J 63:353–365

    Article  CAS  PubMed  Google Scholar 

  • Zakrzewski F, Wenke T, Holtgräwe D et al. (2010) Analysis of a c0t-1 library enables the targeted identification of minisatellite and satellite families in Beta vulgaris. BMC Plant Biol 10:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Zakrzewski F, Weisshaar B, Fuchs J et al. (2011) Epigenetic profiling of heterochromatic satellite DNA. Chromosoma 120:409–422

    Article  PubMed  Google Scholar 

  • Zakrzewski F, Weber B, Schmidt T (2013) A molecular cytogenetic analysis of the structure, evolution, and epigenetic modifications of major DNA sequences in centromeres of Beta species. In: Plant centromere biology. Wiley-Blackwell, Oxford, pp 39–55

    Google Scholar 

  • Zakrzewski F, Schubert V, Viehoever P et al. (2014) The CHH motif in sugar beet satellite DNA: a modulator for cytosine methylation. Plant J 78:937–950

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Henderson IR, Lu C et al. (2007) Role of RNA polymerase IV in plant small RNA metabolism. Proc Natl Acad Sci U S A 104:4536–4541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Lee HR, Koo DH et al. (2008) Epigenetic modification of centromeric chromatin: hypomethylation of DNA sequences in the CENH3-associated chromatin in Arabidopsis thaliana and maize. Plant Cell 20:25–34

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by the BMBF grant “AnnoBeet: Annotation des Genoms der Zuckerrübe unter Berücksichtigung von Genfunktionen und struktureller Variabilität für Nutzung von Genomdaten in der Pflanzenbiotechnologie.”, FKZ-0315962-C to Thomas Schmidt.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas Schmidt .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Zakrzewski, F., Schmidt, T. (2017). Epigenetic Characterization of Satellite DNA in Sugar Beet (Beta vulgaris). In: Rajewsky, N., Jurga, S., Barciszewski, J. (eds) Plant Epigenetics. RNA Technologies. Springer, Cham. https://doi.org/10.1007/978-3-319-55520-1_22

Download citation

Publish with us

Policies and ethics