Skip to main content
SpringerLink
Log in

Molecular structure and chromosome distribution of three repetitive DNA families in Anemone hortensis L. (Ranunculaceae)

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

The structure, abundance and location of repetitive DNA sequences on chromosomes can characterize the nature of higher plant genomes. Here we report on three new repeat DNA families isolated from Anemone hortensis L.; (i) AhTR1, a family of satellite DNA (stDNA) composed of a 554–561 bp long EcoRV monomer; (ii) AhTR2, a stDNA family composed of a 743 bp long HindIII monomer and; (iii) AhDR, a repeat family composed of a 945 bp long HindIII fragment that exhibits some sequence similarity to Ty3/gypsy-like retroelements. Fluorescence in-situ hybridization (FISH) to metaphase chromosomes of A. hortensis (2n = 16) revealed that both AhTR1 and AhTR2 sequences co-localized with DAPI-positive AT-rich heterochromatic regions. AhTR1 sequences occur at intercalary DAPI bands while AhTR2 sequences occur at 8–10 terminally located heterochromatic blocks. In contrast AhDR sequences are dispersed over all chromosomes as expected of a Ty3/gypsy-like element. AhTR2 and AhTR1 repeat families include polyA- and polyT-tracks, AT/TA-motifs and a pentanucleotide sequence (CAAAA) that may have consequences for chromatin packing and sequence homogeneity. AhTR2 repeats also contain TTTAGGG motifs and degenerate variants. We suggest that they arose by interspersion of telomeric repeats with subtelomeric repeats, before hybrid unit(s) amplified through the heterochromatic domain. The three repetitive DNA families together occupy ∼10% of the A. hortensis genome. Comparative analyses of eight Anemone species revealed that the divergence of the A. hortensis genome was accompanied by considerable modification and/or amplification of repeats.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AhDR:

Anemone hortensis dispersed repeats

AhTR:

Anemone hortensis tandem repeats

BLAST:

basic local alignment research tool

CDP:

star detection module

CMA:

chromomycin A3

DAPI:

4′,6-diamidino-2-phenylindole

DIG DNA:

digoxigenin DNA

EDF FISH:

extended DNA fibre FISH

EDTA:

ethylenediaminetetraacetic acid

FISH:

fluorescence in-situ hybridization

FITC:

fluoroscein isothiocyanate

JNK:

Japanese landrace

NCBI:

National Centre for Biotechnology Information

PCR:

polymerase chain reaction

PNA:

peptide nucleic acid

SDS:

sodium dodecyl sulfate

SSC:

standard saline citrate

stDNA:

satellite DNA

TRF:

terminal restriction fragment

References

  • Bernet GP, Asíns MJ (2003) Identification and genomic distribution of gypsy like retrotransposons in Citrus and Poncirus. Theor Appl Genet 108:121–130

    Article  PubMed  CAS  Google Scholar 

  • Bůžek J, Koutníková H, Houben A et al (1997) Isolation and characterization of X chromosome-derived DNA sequences from a dioecious plant Melandrium album. Chromosome Res 5:57–65

    Article  PubMed  Google Scholar 

  • Chen CM, Wang CT, Wang CJ, Ho CH, Kao YY, Chen CC (1997) Two tandemly repeated telomere-associated sequences in Nicotiana plumbaginifolia. Chromosome Res 5:561–568

    Article  PubMed  CAS  Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995

    Article  PubMed  CAS  Google Scholar 

  • Clarkson JJ, Lim KY, Kovarik A, Chase MW, Knapp S, Leitch AR (2005) Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytol 168:241–252

    Article  PubMed  CAS  Google Scholar 

  • Cohn M, Edström JE (1992) Telomere-associated repeats in Chironomus form discrete subfamilies generated by gene conversion. J Mol Evol 35:114–122

    Article  PubMed  CAS  Google Scholar 

  • Cowan CR, Carlton PM, Cande WZ (2001) The polar arrangement of telomeres in interphase and meiosis. Rabl organization and the bouquet. Plant Physiol 125:532–538

    Article  PubMed  CAS  Google Scholar 

  • Cox AV, Bennett ST, Parokonny AS, Kenton A, Callimasia MA, Bennett MD (1993) Comparison of plant telomere locations using a PCR-generated synthetic probe. Ann Bot 72:239–247

    Article  CAS  Google Scholar 

  • Cullis CA, Schweizer D (1974) Repetitious DNA in some Anemone species. Chromosoma 44:417–421

    Article  CAS  Google Scholar 

  • Dechyeva D, Schmidt T (2006) Molecular organization of terminal repetitive DNA in Beta species. Chromosome Res 14:881–897

    Article  PubMed  CAS  Google Scholar 

  • Dover G (1982) Molecular drive a cohesive mode of species evolution. Nature 299:111–117

    Article  PubMed  CAS  Google Scholar 

  • Ehrendorfer F, Samuel R (2001) Contributions to a molecular phylogeny and systematic of Anemone and related genera (Ranunculaceae-Anemoninae). Acta Phytotaxon Sin 39:293–307

    Google Scholar 

  • Fajkus J, Kovarik A, Kralovics R, Bezdek M (1995) Organization of telomeric and subtelomeric chromatin in the higher plant Nicotiana tabacum. Mol Gen Genet 247:633–638

    Article  PubMed  CAS  Google Scholar 

  • Fajkus J, Leitch AR, Chester M, Sýkorová E (2008) Evolution, composition and functions of telomeres and subtelomeres: lessons from plants. In: Nosek J, Tomáska L′u eds. Origin and Evolution of Telomeres. Neuveden, USA: Landes Biosciences, pp. 114–127

  • Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051

    Article  PubMed  CAS  Google Scholar 

  • Ganal MW, Lapitan NLV, Tanksley SD (1991) Macrostructure of the tomato telomeres. Plant Cell 3:87–94

    Article  PubMed  CAS  Google Scholar 

  • Garrido-Ramos MA, de la Herrán R, Ruiz Rejón M, Ruiz Rejón C (1999) A subtelomeric satellite DNA family isolated from the genome of the dioecious plant Silene latifolia. Genome 42:442–446

    Article  PubMed  CAS  Google Scholar 

  • Gilles CB (1984) The synaptonemal complex in higher plants. Critical Rev Plant Sci 2:81–116

    Article  Google Scholar 

  • Gilles CB, Dollin AE, Dai K (1989) Chromosomal and genetic factors influencing synaptonemal complex formation. In: Fredga K, Kihlman BA, Bennett MD (eds) Chromosomes today. Unwin Hyman Ltd, London, pp. 297–310

    Google Scholar 

  • Hagemann S, Scheer B, Schweizer D (1993) Repetitive sequences in the genome of Anemone blanda: Identification of tandem arrays and dispersed repeats. Chromosoma 102:312–324

    Article  PubMed  CAS  Google Scholar 

  • Hall T (1999) BioEdit v5.0.9. North Carolina State University

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

    Article  Google Scholar 

  • Higashiyama T, Noutoshi Y, Akiba M, Yamada T (1995) Telomere and LINE-like elements at the termini of the Chlorella chromosome I. Nucleic Acids Symp Ser 34:71–72

    PubMed  CAS  Google Scholar 

  • Hoot SB (1995) Phylogenetic relationships in Anemone (Ranunculaceae) based on DNA restriction site variation and morphology. Plant Syst Evol 9(Suppl):295–300

    Google Scholar 

  • Hoot SB, Reznicek AA, Palmer JD (1994) Phylogenetic relationships in Anemone (Ranunculaceae) based on morphology and chloroplast DNA. Syst Bot 19:169–200

    Article  Google Scholar 

  • Hudakova S, Michalek W, Presting GG et al (2001) Sequence organization of barley centromeres. Nucleic Acids Res 29:5029–5035

    Article  PubMed  CAS  Google Scholar 

  • Ijdo JW, Wells RA, Baldini A, Reeders ST (1991) Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res 19:545

    Article  Google Scholar 

  • Kishii M, Nagaki K, Tsujimoto H, Sasakuma T (1999) Exclusive localization of tandem repetitive sequences in subtelomeric heterochromatin regions of Leymus racemosus (Poaceae, Triticeae). Chromosome Res 7:519–529

    Article  PubMed  CAS  Google Scholar 

  • Kojima KK, Kubo Y, Fujiwara H (2002) Complex and tandem repeat structure of subtelomeric regions in the Taiwan cricket, Teleogryllus taiwanemma. J Mol Evol 54:474–485

    Article  PubMed  CAS  Google Scholar 

  • Koukalova B, Reich J, Matyasek R, Kuhrova V, Bezdek M (1989) A BamHI family of highly repeated DNA sequences of Nicotiana tabacum. Theor Appl Genet 78:77–80

    Article  CAS  Google Scholar 

  • Kubis S, Heslop-Harrison JS, Schmidt T (1997) A family of differentially amplified repetitive DNA sequences in the genus Beta reveals genetic variation in Beta vulgaris subspecies and cultivars. J Mol Evol 44:310–320

    Article  PubMed  CAS  Google Scholar 

  • Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532

    Article  PubMed  CAS  Google Scholar 

  • Lim KY, Matyasek R, Lichtenstein CP, Leitch AR (2000) Molecular cytogenetic analyses and phylogenetic studies in the Nicotiana section Tomentosae. Chromosoma 109:245–258

    Article  PubMed  CAS  Google Scholar 

  • Lim KY, Kovarik A, Matyasek R et al (2006) Comparative genomics and repetitive sequence divergence in the species of dipoid Nicotiana section Alatae. Plant J 48:907–919

    Article  PubMed  CAS  Google Scholar 

  • Macas J, Mészáros T, Nouzová M (2002) PlantSat: a specialized database for plant satellite repeats. Bioinformatics 18:28–35

    Article  PubMed  CAS  Google Scholar 

  • Macas J, Neumann P, Navrátilová A (2007) Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics 8:427

    Article  PubMed  Google Scholar 

  • Marie D, Brown SC (1993) A cytometric exercise in plant DNA histograms, with 2C values of 70 species. Biol Cell 78:41–51

    Article  PubMed  CAS  Google Scholar 

  • Marks GE, Schweizer D (1974) Giemsa banding: karyotype differences in some species of Anemone and in Hepatica nobilis. Chromosoma 44:405–416

    Article  Google Scholar 

  • Mlinarec J, Papeš D, Besendorfer V (2006) Ribosomal, telomeric and heterochromatin sequences localization in the karyotype of Anemone hortensis. Bot J Linn Soc 150:177–186

    Article  Google Scholar 

  • Nagaki K, Tsujimoto H, Sasakuma T (1999) A novel repetitive sequence, termed the JNK repeat family, located on an extra heterochromatic region of chromosome 2R of Japanese rye. Chromosome Res 6:95–101

    Article  Google Scholar 

  • Neumann P, Nouzová M, Macas J (2001) Molecular and cytogenetic analysis of repetitive DNA in pea (Pisum sativum L.). Genome 44:716–728

    Article  PubMed  CAS  Google Scholar 

  • Ohmido N, Kijima K, Akiyama Y, de Jong JH, Fukui K (2000) Quantification of total genomic DNA and selected repetitive sequences reveals concurrent changes in different DNA families in indica and japonica rice. Mol Gen Genet 263:388–394

    Article  PubMed  CAS  Google Scholar 

  • Palladino F, Gasser SM (1994) Telomere maintenance and gene repression: a common end? Curr Opin Cell Biol 6:373–379

    Article  PubMed  CAS  Google Scholar 

  • Petit M, Lim KY, Julio E et al (2007) Differential impact of retrotransposon populations on the genome of allotetraploid tobacco (Nicotiana tabacum). Mol Gen Genet 278:1–15

    CAS  Google Scholar 

  • Pich U, Schubert I (1998) Terminal heterochromatin and alternative telomeric sequences in Allium cepa. Chromosome Res 6:315–321

    Article  PubMed  CAS  Google Scholar 

  • Pryde FE, Louis EJ (1999) Limitations of silencing at native yeast telomeres. EMBO J 18:2538–2550

    Article  PubMed  CAS  Google Scholar 

  • Puizina J, Weiss-Schneeweiss H, Pedrosa-Harand A et al (2003) Karyotype analysis in Hyacinthella dalmatica (Hyacinthaceae) reveals vertebrate-type telomere repeats at the chromosome ends. Genome 46:1070–1076

    Article  PubMed  CAS  Google Scholar 

  • Riha K, Fajkus J, Siroky J, Vyskot B (1998) Developmental control of telomere lengths and telomerase activity in plants. Plant Cell 10:1691–1698

    Article  PubMed  CAS  Google Scholar 

  • Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphism in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014–8019

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor: New York, pp 6.33–6.64

    Google Scholar 

  • Saunders VA, Houben A (2001) The pericentromeric heterochromatin of the grass Zingeria biebersteiniana (2n = 4) is composed of Zbcen1-type tandem repeats that are intermingled with accumulated dispersedly organized sequences. Genome 44:955–961

    Article  PubMed  CAS  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, Kubis S, Katsiotis A, Jung C, Heslop-Harrison JS (1998) Molecular and chromosomal organization of two repetitive DNA sequences with intercalary locations in sugar beet and other Beta species. Theor Appl Genet 97:696–704

    Article  CAS  Google Scholar 

  • Schuettpelz E, Hoot SB, Samuel R, Ehrendorfer F (2002) Multiple origins of Southern hemisphere Anemone (Ranunculaceae) based on plastid and nuclear sequence data. Plant Syst Evol 231:143–151

    Article  CAS  Google Scholar 

  • Scoles GJ, Gill BS, Xin Z-Y et al (1988) Frequent duplication and deletion events in the 5S RNA genes and the associated space regions of the Triticae. Plant Syst Evol 160:105–122

    Article  CAS  Google Scholar 

  • Sharma S, Raina SN (2005) Organization and evolution of highly repeated satellite DNA sequences in plant chromosomes. Cytogenet Genome Res 109:15–26

    Article  PubMed  CAS  Google Scholar 

  • Singh RJ (2003) Plant cytogenetics. CRC Press, London

    Google Scholar 

  • Skalická K, Lim KY, Matyasek R, Matzke M, Leitch AR, Kovarik A (2005) Preferential elimination of repeated DNA sequences from the paternal, Nicotiana tomentosiformis genome donor of a synthetic, allotetraploid tobacco. New Phytol 166:291–303

    Article  PubMed  Google Scholar 

  • Soler C, García P, Jouve N (1990) Meiotic expression of modified chromosome constitution and structure in x Tritiosecale Wittmack. Heredity 65:21–28

    Article  Google Scholar 

  • Staginnus C, Winter P, Desel C, Schmidt T, Kahl G (1999) Molecular structure and chromosomal localization of major repetitive DNA families in the chickpea (Cicer arietinum L.) genome. Plant Mol Biol 39:1037–1050

    Article  PubMed  CAS  Google Scholar 

  • Suoniemi A, Tanskanen J, Schulman AH (1998) Gypsy-like retrotransposons are widespread in the plant kingdom. Plant J 13:699–705

    Article  PubMed  CAS  Google Scholar 

  • Sýkorová E, Fajkus J, Ito M, Fukui K (2001) Transition between two forms of heterochromatin at plant subtelomeres. Chromosome Res 9:309–323

    Article  PubMed  Google Scholar 

  • Sýkorová E, Cartagena J, Horakova M, Fukui K, Fajkus J (2003a) Characterization of telomere-subtelomere junctions in Silene latifolia. Mol Genet Genomics 269:13–20

    PubMed  Google Scholar 

  • Sýkorová E, Lim KY, Kunicka Z et al (2003b) Telomere variability in the monocotyledonous plant order Asparagales. Proc R Soc Lond B 270:1893–1904

    Article  Google Scholar 

  • Taketa S, Ando H, Takeda K, Harrison GE, Heslop-Harrison JS (2000) The distribution, organization and evolution of two abundant and widespread repetitive DNA sequences in the genus Hordeum. Theor Appl Genet 100:169–176

    Article  CAS  Google Scholar 

  • Tamura M (1995) Angiospermae: Ordnung Ranunculales, Fam. Ranunculaceae. In: Engler A, Prantl K, eds. Die Natürlichen Pflanzenfamilien. ed. 2 (Hiepko P ed.). 17aIV. Berlin: Duncker and Humblot, pp. 1–555

  • Tek AL, Jiang J (2004) The centromeric regions of potato chromosomes contain megabase-sized tandem arrays of telomere-similar sequences. Chromosoma 113:77–83

    Article  PubMed  CAS  Google Scholar 

  • Tek AL, Song J, Macas J, Jiang J (2005) Sobo, a recently amplified satellite repeat of potato, and its implications for the origin of tandemly repeated sequences. Genetics 170:1231–1238

    Article  PubMed  CAS  Google Scholar 

  • Thomson KG, Thomas JE, Dietzgen RG (1998) Retrotransposon-like sequences integrated into the genome of pineapple Ananas comosus. Plant Mol Biol 38:461–465

    Article  PubMed  CAS  Google Scholar 

  • Vershinin AV, Heslop-Harrison JS (1998) Comparative analysis of the nucleosomal structure of rye, wheat and their relatives. Plant Mol Biol 36:149–161

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Tang X, Cheng Z, Mueller L, Giovannoni J, Tanksley SD (2006) Euchromatin and pericentromeric heterochromatin: comparative composition in the tomato genome. Genetics 172:2529–2540

    Article  PubMed  CAS  Google Scholar 

  • Weiss H, Schertan H (2002) Aloe spp.-plants with vertebrate-like telomeric sequences. Chromosome Res 10:155–164

    Article  PubMed  CAS  Google Scholar 

  • Weiss-Schneeweiss H, Riha K, Jang CG, Puizina J, Schertan H, Schweizer D (2004) Chromosome termini of the monocot plant Othocallis siberica are maintained by telomerase, which specifically synthesizes vertebrate-type telomere sequences. Plant J 37:484–493

    Article  PubMed  CAS  Google Scholar 

  • Zhong XB, Fransz PF, Wennekes-van Eden J et al (1998) FISH studies reveal the molecular and chromosomal organization of individual telomere domains in tomato. Plant J 13:507–517

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to K. Riha from the Gregor Mendel Institute, Vienna for the help in TRF analysis. V.B. thanks J. Puizina for helpful suggestions during the preparation of the manuscript. This work was funded by the Ministry of Science, Education and Sport of the Republic of Croatia, grants 119112 and 119-1191196-1201 and British Scholarship Trust foundation that funded training of J.M. at Queen Mary University of London.

Author information

Authors and Affiliations

  1. Department of Molecular Biology, Biology Division, Faculty of Science, University of Zagreb, Horvatovac 102a, HR-10000, Zagreb, Croatia

    Jelena Mlinarec, Dražena Papeš & Višnja Besendorfer

  2. School of Biological and Chemical Sciences, Queen Mary University of London, London, UK

    Mike Chester & Andrew R. Leitch

  3. Department of Ecology, Evolution and Systematics, UMR CNRS 8079, University Paris-Sud, Orsay Cedex, France

    Sonja Siljak-Yakovlev

Authors
  1. Jelena Mlinarec
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mike Chester
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sonja Siljak-Yakovlev
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dražena Papeš
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrew R. Leitch
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Višnja Besendorfer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Višnja Besendorfer.

Additional information

Responsible Editor: Pat Heslop-Harrison.

Electronic supplementary material

Below is the image is a link to a high resolution version.

Supplementary Fig. S1

Alignment of cloned repeated units. Sequences have a high A+T content (66–69%) and 81–87% sequence similarity. Internal motifs that are repeated are boxed in red, green and blue. KpnI restriction site and pentanucleotide CAAAA motif are underlined (JPG 980 kb)

Supplementary Fig. S2

Primary structure of AhTR2-1 repetitive sequence with TTTAGGG motifs and degenerate variants (boxed) and pentanucleotide CAAAA sequence (underlined). Arrows indicate primer pair AhTR2-1 and AhTR2-2 used for PCR amplification of AhTR2 sequence family (JPG 582 kb)

Supplementary Fig. S3

Sequence alignment of 8 subtelomeric AhTR2 clones (AhTR2-2-AhTR2-10) obtained by PCR amplification and AhTR2-1 HindIII fragment from A. hortensis. Short deletions/amplifications are present in the region with TTTAGGG tandem repeats (boxed) (JPG 2.74 MB)

Supplementary Fig. S4

Sequences having regions of high levels of similarity with reverse transcriptase/RNaseH (RTH) and integrase (INT) of the Ty3/gypsy-like retrotransposon, areas boxed (JPG 1.03 MB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mlinarec, J., Chester, M., Siljak-Yakovlev, S. et al. Molecular structure and chromosome distribution of three repetitive DNA families in Anemone hortensis L. (Ranunculaceae). Chromosome Res 17, 331–346 (2009). https://doi.org/10.1007/s10577-009-9025-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-009-9025-2

Keywords

Search

Navigation