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Telomere and 45S rDNA sequences are structurally linked on the chromosomes in Chrysanthemum segetum L.

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Abstract

Some reports have shown that nucleolar organizer regions are located at the telomeric region and have a structural connection with telomeres at the cellular level in many organisms. In this study, we found that all 45S ribosomal DNA (rDNA) signals were located at telomeric regions on the chromosomes in Chrysanthemum segetum L., and the 45S rDNA showed distinct signal patterns on different metaphase chromosome spreads. The bicolor fluorescence in situ hybridization experiment on the extended fibers revealed that telomere repeats were structurally connected with or interspersed into rDNA sequences. The close cytological structure relation between rDNA and telomere sequences led us to use PCR with combinations of the telomere primer and the rDNA primer to obtain some fragments, which were flanked by different rDNA and telomere primer sequences. One representative clone CHS2 contains closely connected rDNA and telomere sequences, suggesting that the telomere sequence invaded into the conserved rDNA sequence. In addition, the sequences of some PCR clones were flanked by the single telomeric primer sequence or the rDNA primer sequence. These results suggested that homologous recombination occurred between tandem repeat units of rDNA sequences or telomere repeats at the chromosome terminus.

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Abbreviations

ALT:

Alternative lengthening of telomeres

DSB:

Double-strand breakage

FISH:

Fluorescence in situ hybridization

ITRs:

Interstitial telomere repeats

ITS:

Internal transcribed spacer

NORs:

Nucleolar organizer regions

References

  • Alvarez-Castellanos PP, Bishop CD, Pascual-Villalobos MJ (2001) Antifungal activity of the essential oil of flowerheads of garland chrysanthemum (Chrysanthemum coronarium) against agricultural pathogens. Phytochemistry 57:99–102

    Article  PubMed  CAS  Google Scholar 

  • Armstrong SJ, Franklin FC, Jones GH (2001) Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J Cell Sci 114:4207–4217

    PubMed  CAS  Google Scholar 

  • Azzalin CM, Nergadze SG, Giulotto E (2001) Human intrachromosomal telomeric-like repeats: sequence organization and mechanisms of origin. Chromosoma 110:75–82

    Article  PubMed  CAS  Google Scholar 

  • Caperta AD, Neves N, Viegas W, Pikaard CS, Preuss S (2007) Relationships between transcription, silver staining, and chromatin organization of nucleolar organizers in Secale cereale. Protoplasma 232: 55-59

    Google Scholar 

  • Castiglione MR, Venora G, Ravalli C, Stoilov L, Gecheff K, Cremonini R (2008) DNA methylation and chromosomal rearrangements in reconstructed karyotypes of Hordeum vulgare L. Protoplasma 232: 215-222

    Google Scholar 

  • Copenhaver GP, Pikaard CS (1996) RFLP and physical mapping with an rDNA-specific endonuclease reveals that nucleolus organizer regions of Arabidopsis thaliana adjoin the telomeres on chromosomes 2 and 4. Plant J 9:259–272

    Article  PubMed  CAS  Google Scholar 

  • Dobigny G, Ozouf-Costaz C, Bonillo C, Volobouev V (2003) Evolution of rRNA gene clusters and telomeric repeats during explosive genome repatterning in Taterillus X (Rodentia, Gerbillinae). Cytogenet Genome Res 103:94–103

    Article  PubMed  CAS  Google Scholar 

  • Dvorácková M, Rossignol P, Shaw PJ, Koroleva OA, Doonan JH, Fajkus J (2010) AtTRB1, a telomeric DNA-binding protein from Arabidopsis, is concentrated in the nucleolus and shows highly dynamic association with chromatin. Plant J 61:637–649

    Article  PubMed  Google Scholar 

  • Fajkus J, Sykorová E, Leitch AR (2005) Telomeres in evolution and evolution of telomeres. Chromosome Res 13:469–479

    Article  PubMed  CAS  Google Scholar 

  • Fajkus J, Leitch AR, Chester M, Sýkorová E (2008) Evolution, composition and interrelated functions of telomeres and subtelomeres: lesson from plants. In: Nosek J, Tomaska L (eds) Origin and evolution of telomeres. Landes Bioscience, Austin, pp 114–127

    Google Scholar 

  • Garcia S, Garnatje T, Pellicer J, McArthur ED, Siljak-Yakovlev S, Vallès J (2009) Ribosomal DNA, heterochromatin, and correlation with genome size in diploid and polyploid North American endemic sagebrushes (Artemisia, Asteraceae). Genome 52:1012–1024

    Article  PubMed  CAS  Google Scholar 

  • Hasterok R, Jenkins G, Langdon T, Jones RN, Maluszynska J (2001) Ribosomal DNA is an effective marker of Brassica chromosomes. Theor Appl Genet 103:486–490

    Article  CAS  Google Scholar 

  • Huang J, Brito IL, Villen J, Gygi SP, Amon A, Moazed D (2006) Inhibition of homologous recombination by a cohesin-associated clamp complex recruited to the rDNA recombination enhancer. Genes Dev 20:2887–2901

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Ma L, Yang F, Fei S, Li L (2008) 45S rDNA regions are chromosome fragile sites expressed as gaps in vitro on metaphase chromosomes of root-tip meristematic cells in Lolium spp. PLoS One 3:e2167

    Article  PubMed  Google Scholar 

  • Huang J, Ma L, Sundararajan S, Fei SZ, Li L (2009) Visualization by atomic force microscopy and FISH of the 45S rDNA gaps in mitotic chromosomes of Lolium perenne. Protoplasma 236:59–65

    Article  PubMed  CAS  Google Scholar 

  • Li LJ, Arumuganathan K, Rines HW, Phillips RL, Riera-Lizarazu O, Sandhu D, Zhou Y, Gill KS (2001) Flow cytometric sorting of maize chromosome 9 from an oat–maize chromosome addition line. Thero Appl Genet 102:658–663

    Article  CAS  Google Scholar 

  • Li L, Yang J, Tong Q, Zhao L, Song Y (2005) A novel approach to prepare extended DNA fibers in plants. Cytom A 63:114–117

    Article  CAS  Google Scholar 

  • Linardopoulou EV, Williams EM, Fan Y, Friedman C, Young JM, Trask BJ (2005) Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature 437: 94–100

    Google Scholar 

  • Liu WS, Fredga K (1999) Telomeric (TTAGGG) n sequences are associated with nucleolus organizer regions (NORs) in the wood lemming. Chromosome Res 7:235–240

    Article  PubMed  CAS  Google Scholar 

  • Manevski A, Bertoni G, Bardet C, Tremousaygue D, Lescure B (2000) In synergy with various cis-acting elements, plant insterstitial telomere motifs regulate gene expression in Arabidopsis root meristems. FEBS Lett 483:43–46

    Article  PubMed  CAS  Google Scholar 

  • Meyne J, Baker RJ, Hobart HH, Hsu TC, Ryder OA, Ward OG, Wiley JE, Wurster-Hill DH, Yates TL, Moyzis RK (1990) Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma 99:3–10

    Article  PubMed  CAS  Google Scholar 

  • Nergadze SG, Rocchi M, Azzalin CM, Mondello C, Giulotto E (2004) Insertion of telomeric repeats at intrachromosomal break sites during primate evolution. Genome Res 14:1704–1710

    Article  PubMed  CAS  Google Scholar 

  • Nosek J, Kosa P, Tomaska L (2006) On the origin of telomeres: a glimpse at the pre-telomerase world. BioEssays 28:182–190

    Article  PubMed  CAS  Google Scholar 

  • Ochocka RJ, Rajzer D, Kowalski P, Lamparczyk H (1995) Determination of coumarins from Chrysanthenum segetum L. by capillary electrophoresis. J Chromatogr A 709:197–202

    Article  CAS  Google Scholar 

  • Perez MP, Navas-Cortes JA, Pascual-Villalobos MJ, Castillo P (2003) Nematicidal activity of essential oils and organic amendments from Asteraceae against root-knot nematodes. Plant Pathol 52:395–401

    Article  Google Scholar 

  • Pich U, Fuchs J, Schubert I (1996) How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences? Chromosome Res 4:207–213

    Article  PubMed  CAS  Google Scholar 

  • Preuss S, Pikaard CS (2007) rRNA gene silencing and nucleolar dominance: insights into a chromosome-scale epigenetic on/off switch. Biochim Biophys Acta 1769:383–392

    PubMed  CAS  Google Scholar 

  • Rakotoarisoa G, Hirai Y, Go Y, Kawamoto Y, Shima T, Koyama N, Randrianjafy A, Mora R, Hirai H (2000) Chromosomal localization of 18S rDNA and telomere sequence in the aye-aye, Daubentonia madagascariensis. Genes Genet Syst 75:299–303

    Article  PubMed  CAS  Google Scholar 

  • Richard GF, Paques F (2000) Mini-and microsatellite expansions: the recombination connection. EMBO Rep 1:122–126

    Article  PubMed  CAS  Google Scholar 

  • Rudd MK, Friedman C, Parghi SS, Linardopoulou EV, Hsu L, Trask BJ (2007) Elevated Rates of Sister Chromatid Exchange at Chromosome Ends. PLoS Genet 3: e32

  • Ruiz-Herrera A, García F, Giulotto E, Attolini C, Egozcue J, Ponsà M, Garcia M (2005) Evolutionary breakpoints are co-localized with fragile sites and intrachromosomal telomeric sequences in primates. Cytogenet Genome Res 108:234–247

    Article  PubMed  CAS  Google Scholar 

  • Schubert I, Wobus U (1985) In situ hybridization confirms jumping nucleolus organizing regions in Allium. Chromosoma 92:143–148

    Article  Google Scholar 

  • Sýkorová E, Fajkus J, Mezníková M, Lim KY, Neplechová K, Blattner FR, Chase MW, Leitch AR (2006) Minisatellite telomeres occur in the family Alliaceae but are lost in Allium. Am J Bot 93:814–823

    Article  PubMed  Google Scholar 

  • Thomas HM, Harper JA, Morgan WG (2001) Gross chromosome rearrangements are occurring in an accession of the grass Lolium rigidum. Chromosome Res 9:585–590

    Article  PubMed  CAS  Google Scholar 

  • Tsujimoto H (1999) De novo synthesis of telomere sequences at the healed breakpoints of wheat deletion chromosomes. Mol Genet Genomics 262:851–856

    Article  CAS  Google Scholar 

  • Tsujimoto H, Yamada T, Sasakuma T (1997) Molecular structure of a wheat chromosome end healed after gametocidal gene-induced breakage. Proc Natl Acad Sci USA 94:3140–3144

    Article  PubMed  CAS  Google Scholar 

  • Upcroft JA, Abedinia M, Upcroft P (2005) Rearranged subtelomeric rRNA genes in Giardia duodenalis. Eukaryot Cell 4:484–486

    Article  PubMed  CAS  Google Scholar 

  • Yu W, Lamb JC, Han F, Birchler JA (2006) Telomere-mediated chromosomal truncation in maize. Proc Natl Acad Sci USA 103:17331–17336

    Article  PubMed  CAS  Google Scholar 

  • Zhdanova NS, Minina JM, Karamisheva TV, Draskovic I, Rubtsov NB, Londono-Vallejo JA (2007) The very long telomeres in Sorex granarius (Soricidae, Eulipothyphla) contain ribosomal DNA. Chromosome Res 15:881–890

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the NSFC (nos. 30870261 and 30771204), the National Genetically Modified Organism Breeding Major Project (no. 200908010-008B), the Research Fund for the Doctoral Program of Higher Education (no. 20090141110031), and the Fundamental Research Funds for the Central Universities (no. 3081003).

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The authors declare that they have no conflict of interest.

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Correspondence to Lijia Li.

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Li, J., He, S., Zhang, L. et al. Telomere and 45S rDNA sequences are structurally linked on the chromosomes in Chrysanthemum segetum L.. Protoplasma 249, 207–215 (2012). https://doi.org/10.1007/s00709-011-0279-0

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  • DOI: https://doi.org/10.1007/s00709-011-0279-0

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