Skip to main content
Log in

The subtelomeric region of the Arabidopsis thaliana chromosome IIIR contains potential genes and duplicated fragments from other chromosomes

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The subtelomere and a portion of the associated telomeric region (together named 3RTAS) of chromosome IIIR from the Arabidopsis thaliana ecotypes Columbia (Col) and Wassilewskija (Ws) were specifically amplified by polymerase chain reaction and subsequently cloned and sequenced. The centromere-proximal portion of 3RTAS from both ecotypes contained two newly identified potential genes, one encoding the chloroplast luminal 19-kDa protein precursor and the other encoding three potential alternatively spliced CCCH-type zinc finger proteins. The telomere-proximal portion of 3RTAS from the Col ecotype contained short duplicated fragments derived from chromosomes I, II, and III, and that from the Ws ecotype contained a duplicated fragment derived from chromosome V. Each duplicated fragment has diverged somewhat in sequence from that of the ectopic template. Small patches of homologous nucleotides were found within the flanking sequences of both the duplicated fragments and the corresponding ectopic template sequences. The structural characteristics of these duplicated fragments suggest that they are filler DNAs captured by non-homologous end joining during double-strand break repair. Our characterization of 3RTAS not only filled up a gap in the chromosome IIIR sequence of A. thaliana but also identified new genes with unknown functions.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

DIG:

Digoxigenin

DSB:

Double-strand break

NCBI:

National Center for Biotechnology Information

NHEJ:

Non-homologous end joining

PCR:

Polymerase chain reaction

STELA:

Single-telomere length analysis

TAIR:

The Arabidopsis Information Resources

TAS:

Telomere-associated sequence

References

  • Alkhimova OG, Mazurok NA, Potapova TA, Zakian SM, Heslop-Harrison JS, Vershinin AV (2004) Diverse patterns of the tandem repeats organization in rye chromosomes. Chromosoma 113:42–52

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Arneric M, Lingner J (2007) Tel1 kinase and subtelomere-bound Tbf1 mediate preferential elongation of short telomeres by telomerase in yeast. EMBO Rep 8:1080–1085

    Article  CAS  PubMed  Google Scholar 

  • Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J (2007) Telomeric repeat-containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318:798–801

    Article  CAS  PubMed  Google Scholar 

  • Baird DM, Rowson J, Wynford-Thomas D, Kipling D (2003) Extensive allelic variation and ultrashort telomeres in senescent human cells. Nat Genet 33:203–207

    Article  CAS  PubMed  Google Scholar 

  • Baur JA, Zou Y, Shay JW, Wright WE (2001) Telomere position effect in human cells. Science 292:2075–2077

    Article  CAS  PubMed  Google Scholar 

  • Berthiau AS, Yankulov K, Bah A, Revardel E, Luciano P, Wellinger RJ, Geli V, Gilson E (2006) Subtelomeric proteins negatively regulate telomere elongation in budding yeast. EMBO J 25:846–856

    Article  CAS  PubMed  Google Scholar 

  • Carlson M, Celenza JL, Eng FJ (1985) Evolution of the dispersed SUC gene family of Saccharomyces by rearrangements of chromosome telomeres. Mol Cell Biol 5:2894–2902

    CAS  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  CAS  PubMed  Google Scholar 

  • Chen CM, Wang CT, Ho CH (2001) A plant gene encoding a Myb-like protein that binds telomeric GGTTTAG repeats in vitro. J Biol Chem 276:16511–16519

    Article  CAS  PubMed  Google Scholar 

  • Chen CM, Wang CT, Kao YH, Chang GD, Ho CH, Lee FM, Hseu MJ (2005) Functional redundancy of the duplex telomeric DNA-binding proteins in Arabidopsis. Bot Bull Acad Sin 46:315–324

    CAS  Google Scholar 

  • Gorbunova V, Levy AA (1997) Non-homologous DNA end joining in plant cells is associated with deletions and filler DNA insertions. Nucleic Acids Res 25:4650–4657

    Article  CAS  PubMed  Google Scholar 

  • Gottschling DE, Aparicio OM, Billington BL, Zakian VA (1990) Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63:751–762

    Article  CAS  PubMed  Google Scholar 

  • Heacock M, Spangler E, Riha K, Puizina J, Shippen DE (2004) Molecular analysis of telomere fusions in Arabidopsis: multiple pathways for chromosome end-joining. EMBO J 23:2304–2313

    Article  CAS  PubMed  Google Scholar 

  • Hediger F, Berthiau AS, van Houwe G, Gilson E, Gasser SE (2006) Subtelomeric factors antagonize telomere anchoring and Tel1-independent telomere length regulation. EMBO J 25:857–867

    Article  CAS  PubMed  Google Scholar 

  • Kuo HF, Olsen KM, Richards EJ (2006) Natural variation in a subtelomeric region of Arabidopsis: implications for the genomic dynamics of a chromosome end. Genetics 173:401–417

    Article  CAS  PubMed  Google Scholar 

  • Levis RW, Ganesan R, Houtchens K, Tolar LA, Sheen FM (1993) Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75:1083–1093

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Louis EJ (1995) The chromosome ends of Saccharomyces cerevisiae. Yeast 11:1553–1573

    Article  CAS  PubMed  Google Scholar 

  • Ohmido N, Kijima K, Ashikawa I, de Jong JH, Fukui K (2001) Visualization of the terminal structure of rice chromosomes 6 and 12 with multicolor FISH to chromosomes and extended DNA fibers. Plant Mol Biol 47:413–421

    Article  CAS  PubMed  Google Scholar 

  • Pearce SR, Pich U, Harrison G, Flavell AJ, Heslop-Harrison JS, Schubert I, Kumar A (1996) The Ty1-copia group retrotransposons of Allium cepa are distributed throughout the chromosomes but are enriched in the terminal heterochromatin. Chromosome Res 4:357–364

    Article  CAS  PubMed  Google Scholar 

  • Pedram M, Sprung CN, Gao Q, Lo AW, Reynolds GE, Murnane JP (2006) Telomere position effect and silencing of transgenes near telomeres in the mouse. Mol Cell Biol 26:1865–1878

    Article  CAS  PubMed  Google Scholar 

  • Pryde FE, Gorham HC, Louis EJ (1997) Chromosome ends: all the same under their caps. Curr Opin Genet Dev 7:822–828

    Article  CAS  PubMed  Google Scholar 

  • Puchta H (2005) The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. J Exp Bot 56:1–14

    Article  CAS  PubMed  Google Scholar 

  • Richards EJ, Ausubel FM (1988) Isolation of higher eukaryotic telomere from Arabidopsis thaliana. Cell 53:127–136

    Article  CAS  PubMed  Google Scholar 

  • Richards EJ, Elgin SC (2002) Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108:489–500

    Article  CAS  PubMed  Google Scholar 

  • Roder MS, Lapitan NL, Sorrells ME, Tanksley SD (1993) Genetic and physical mapping of barley telomere. Mol Gen Genet 238:294–303

    CAS  PubMed  Google Scholar 

  • Salomon S, Puchta H (1998) Capture of genomic and T-DNA sequences during double-strand break repair in somatic plant cells. EMBO J 17:6086–6095

    Article  CAS  PubMed  Google Scholar 

  • Schoeftner S, Blasco MA (2008) Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol 10:228–236

    Article  CAS  PubMed  Google Scholar 

  • Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277:8354–8365

    Article  CAS  PubMed  Google Scholar 

  • Sharp PA, Burge CB (1997) Classification of introns: U2-type and U12-type. Cell 91:875–879

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Teng SC, Zakian VA (1999) Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol Cell Biol 19:8083–8093

    CAS  PubMed  Google Scholar 

  • Vershinin AV, Schwarzacher T, Heslop-Harrison JS (1995) The large-scale genomic organization of repetitive DNA families at the telomeres of rye chromosomes. Plant Cell 7:1823–1833

    Article  CAS  PubMed  Google Scholar 

  • Vrbsky J, Akimcheva S, Watson JM, Turner TL, Daxinger L, Vyskot B, Aufsatz W, Riha K (2010) siRNA-mediated methylation of Arabidopsis telomeres. PLoS Genetics 6:e1000986. doi:10.1371/journal.pgen.1000986

    Article  PubMed  Google Scholar 

  • Wang D, Guo Y, Wu C, Yang G, Li Y, Zheng C (2008) Genome-wide analysis of CCCH zinc finger family in Arabidopsis and rice. BMC Genomics 9:44. doi:10.1186/1471-2164-9-44

    Article  PubMed  Google Scholar 

  • Wu C, Kim YS, Smith KM, Li W, Hood HM, Staben C, Selker EU, Sachs MS, Farman ML (2009) Characterization of chromosome ends in the filamentous fungus Neurospora crassa. Genetics 181:1129–1145

    Article  CAS  PubMed  Google Scholar 

  • Zakian VA (1995) Telomeres: beginning to understand the end. Science 270:1601–1607

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

We thank the transgenic plant core laboratory at Academia Sinica for providing the picture of Arabidopsis plant shown in the cover page.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chung-Mong Chen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, CT., Ho, CH., Hseu, MJ. et al. The subtelomeric region of the Arabidopsis thaliana chromosome IIIR contains potential genes and duplicated fragments from other chromosomes. Plant Mol Biol 74, 155–166 (2010). https://doi.org/10.1007/s11103-010-9664-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-010-9664-x

Keywords

Navigation