Advertisement

Chromosome Research

, Volume 11, Issue 3, pp 263–275 | Cite as

Telomere structure, function and maintenance in Arabidopsis

  • Karel Riha
  • Dorothy E. Shippen
Article

Abstract

The stability of eukaryotic genomes is provided in part by the integrity of telomeres, the nucleoprotein caps on the ends of chromosome. Recent studies reveal that proper telomere architecture is required for long-term proliferation capacity. Here we describe molecular mechanisms that protect and maintain chromosome ends and discuss why Arabidopsis is emerging as a powerful new model for elucidating fundamental aspects of telomere biology.

Arabidopsis DNA repair restriction fragment analysis telomerase telomere TRF 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams SP, Leitch IJ, Bennett MD, Leitch AR (2000) Aloe L.—a second plant family without (TTTAGGG)n telomeres. Chromosoma 109: 201‐205.Google Scholar
  2. Adams SP, Hartman TP, Lim KY et al. (2001) Loss and recovery of Arabidopsis‐type telomere repeat sequences 5'‐(TTTAGGG)(n)‐3' in the evolution of a major radiation of flowering plants. Proc R Soc Lond B Biol Sci 268: 1541‐1546.Google Scholar
  3. Ahmed S, Hodgkin J (2000) MRT‐2 checkpoint protein is required for germline immortality and telomere replication in C. elegans. Nature 403: 159‐164.Google Scholar
  4. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796‐815.Google Scholar
  5. Artandi SE, Chang S, Lee SL et al. (2000) Telomere dysfunction promotes non‐reciprocal translocations and epithelial cancers in mice. Nature 406: 641‐645.Google Scholar
  6. Baumann P, Cech TR (2001) Pot1, the putative telomere end‐binding protein in fission yeast and humans. Science 292: 1171‐1175.Google Scholar
  7. Baumann P, Podell E, Cech TR (2002) Human Pot1 (protection of telomeres) protein: cytolocalization, gene structure, and alternative splicing. Mol Cell Biol 22: 8079‐8087.Google Scholar
  8. Blackburn EH (2000) Telomere states and cell fates. Nature 408: 53‐56.Google Scholar
  9. Blackburn EH (2001) Switching and signaling at the telomere. Cell 106: 661‐673.Google Scholar
  10. Blasco MA, Lee HW, Hande MP et al. (1997) Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91: 25‐34.Google Scholar
  11. Bucholc M, Buchowicz J (1995) An extrachromosomal fragment of telomeric DNA in wheat. Plant Mol Biol 27: 435‐439.Google Scholar
  12. Bucholc M, Park Y, Lustig AJ (2001) Intrachromatid excision of telomeric DNA as a mechanism for telomere size control in Saccharomyces cerevisiae. Mol Cell Biol 21: 6559‐6573.Google Scholar
  13. Bundock P, Hooykaas P (2002) Severe developmental defects, hypersensitivity to DNA‐damaging agents, and lengthened telomeres in Arabidopsis MRE11 mutants. Plant Cell 14: 2451‐2462.Google Scholar
  14. Bundock P, van Attikum H, Hooykaas P (2002) Increased telomere length and hypersensitivity toDNAdamaging agents in an Arabidopsis KU70 mutant. Nucleic Acids Res 30: 3395‐3400.Google Scholar
  15. Cervantes RB, Lundblad V (2002) Mechanisms of chromosome‐end protection. Curr Opin Cell Biol 14: 351‐356.Google Scholar
  16. Chan SW, Chang J, Prescott J, Blackburn EH (2001) Altering telomere structure allows telomerase to act in yeast lacking ATM kinases. Curr Biol 11: 1240‐1250.Google Scholar
  17. Chen JL, Blasco MA, Greider CW (2000) Secondary structure of vertebrate telomerase RNA. Cell 100: 503‐514.Google Scholar
  18. Chen CM, Wang CT, Ho CH (2001) A plant gene encoding a Myb‐like protein that binds telomeric GGTTAG repeats in vitro. J Biol Chem 276: 16511‐16519.Google Scholar
  19. Chin L, Artandi SE, Shen Q et al. (1999) p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 97: 527‐538.Google Scholar
  20. Collins K, Mitchell JR (2002) Telomerase in the human organism. Oncogene 21: 564‐579.Google Scholar
  21. Conrad MN, Wright JH, Wolf AJ, Zakian VA (1990) RAP1 protein interacts with yeast telomeres in vivo: overproduction alters telomere structure and decreases chromosome stability. Cell 63: 739‐750.Google Scholar
  22. Cooper JP, Nimmo ER, Allshire RC, Cech TR (1997) Regulation of telomere length and function by a Myb‐domain protein in fission yeast. Nature 385: 744‐747.Google Scholar
  23. 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.Google Scholar
  24. D'Amours D, Jackson SP (2002) The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat Rev Mol Cell Biol 3: 317‐327.Google Scholar
  25. Diede SJ, Gottschling DE (1999) Telomerase‐mediated telomere addition in vivo requires DNA primase and DNA polymerases alpha and delta. Cell 99: 723‐733.Google Scholar
  26. Dubrana K, Perrod S, Gasser SM (2001) Turning telomeres off and on. Curr Opin Cell Biol 13: 281‐289.Google Scholar
  27. Ducrest AL, Szutorisz H, Lingner J, Nabholz M (2002) Regulation of the human telomerase reverse transcriptase gene. Oncogene 21: 541‐552.Google Scholar
  28. Espejel S, Franco S, Rodriguez‐Perales S, Bouffler SD, Cigudosa JC, Blasco MA (2002) Mammalian Ku86 mediates chromosomal fusions and apoptosis caused by critically short telomeres. EMBO J 21: 2207‐2219.Google Scholar
  29. 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.Google Scholar
  30. Fitzgerald MS, McKnight TD, Shippen DE (1996) Characterization and developmental patterns of telomerase expression in plants. Proc Natl Acad Sci USA 93: 14422‐14427.Google Scholar
  31. Fitzgerald MS, Riha K, Gao F, Ren S, McKnight TD, Shippen DE (1999) Disruption of the telomerase catalytic subunit gene from Arabidopsis inactivates telomerase and leads to a slow loss of telomeric DNA. Proc Natl Acad Sci USA 96: 14813‐14818.Google Scholar
  32. Fitzgerald MS, Shakirov EV, Hood EE, McKnight TD, Shippen DE (2001) Different modes of de novo telomere formation by plant telomerases. Plant J 26: 77‐87.Google Scholar
  33. Fulneckova J, Fajkus J (2000) Inhibition of plant telomerase by telomere‐binding proteins from nuclei of telomerase‐negative tissues. FEBSLett 467: 305‐310.Google Scholar
  34. Gallego ME, White CI (2001) RAD50 function is essential for telomere maintenance in Arabidopsis. Proc Natl Acad Sci USA 98: 1711‐1716.Google Scholar
  35. Gallego ME, Jeanneau M, Granier F, Bouchez D, Bechtold N, White CI (2001) Disruption of the Arabidopsis RAD50 gene leads to plant sterility and MMS sensitivity. Plant J 25: 31‐41.Google Scholar
  36. Garcia V, Salanoubat M, Choisne N, Tissier A (2000) An ATM homologue from Arabidopsis thaliana: complete genomic organisation and expression analysis. Nucleic Acids Res 28: 1692‐1699.Google Scholar
  37. Greider CW (1996) Telomere length regulation. Annu Rev Biochem 65: 337‐365.Google Scholar
  38. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, de Lange T (1999) Mammalian telomeres end in a large duplex loop. Cell 97: 503‐514.Google Scholar
  39. Heller K, Kilian A, Piatyszek MA, Kleinhofs A (1996) Telomerase activity in plant extracts. Mol Gen Genet 252: 342‐345.Google Scholar
  40. Heller‐Uszynska K, Schnippenkoetter W, Kilian A (2002) Cloning and characterization of rice (Oryza sativa L) telomerase reverse transcriptase, which reveals complex splicing patterns. Plant J 31: 75‐86.Google Scholar
  41. Herrera E, Samper E, Blasco MA (1999) Telomere shortening in mTR–/–embryos is associated with failure to close the neural tube. EMBO J 18: 1172‐1181.Google Scholar
  42. Higashiyama T, Maki S, Yamada T (1995) Molecular organization of Chlorella vulgaris chromosome I: presence of telomeric repeats that are conserved in higher plants. Mol Gen Genet 246: 29‐36.Google Scholar
  43. Ishikawa F, Naito T (1999) Why do we have linear chromosomes? A matter of Adam and Eve. Mutation Res 434: 99‐107.Google Scholar
  44. Kilian A, Stiff C, Kleinhofs A (1995) Barley telomeres shorten during differentiation but grow in callus culture. Proc Natl Acad Sci USA 92: 9555‐9559.Google Scholar
  45. Kilian A, Heller K, Kleinhofs A (1998) Development patterns of telomerase activity in barley and maize. Plant Mol Biol 37: 621‐628.Google Scholar
  46. Kim JH, Kim WT, Chung IK (1998) Rice proteins that bind single‐stranded G‐rich telomere DNA. Plant Mol Biol 36: 661‐672.Google Scholar
  47. Klobutcher LA, Swanton MT, Donini P, Prescott DM (1981) All gene‐sized DNA molecules in four species of hypotrichs have the same terminal sequence and an unusual 3' terminus. Proc Natl Acad Sci USA 78: 3015‐3019.Google Scholar
  48. Lee HW, Blasco MA, Gottlieb GJ, Horner JW, 2nd, Greider CW, DePinho RA (1998) Essential role of mouse telomerase in highly proliferative organs. Nature 392: 569‐574.Google Scholar
  49. Lee JH, Kim JH, Kim WT, Kang BG, Chung IK (2000) Characterization and developmental expression of single‐stranded telomeric DNA‐binding proteins from mung bean (Vigna radiata). Plant Mol Biol 42: 547‐557.Google Scholar
  50. Li B, Oestreich S, de Lange T (2000) Identification of human Rap1: implications for telomere evolution. Cell 101: 471‐483.Google Scholar
  51. Li H, Zhao L, Yang Z, Funder JW, Liu JP (1998) Telomerase is controlled by protein kinase C‐alpha in human breast cancer cells. J Biol Chem 273: 33436‐33442.Google Scholar
  52. Lingner J, Hendrick LL, Cech TR (1994) Telomerase RNAs of different ciliates have a common secondary structure and a permuted template. Genes Dev 8: 1984‐1998.Google Scholar
  53. Lingner J, Cooper JP, Cech TR (1995) Telomerase and DNA end replication: no longer a lagging strand problem? Science 269: 1533‐1534.Google Scholar
  54. Lysak MA, Fransz PF, Ali HB, Schubert I (2001) Chromosome painting in Arabidopsis thaliana. Plant J 28: 689‐697.Google Scholar
  55. Makarov VL, Hirose Y, Langmore JP (1997) Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell 88: 657‐666.Google Scholar
  56. Maringele L, Lydall D (2002) EXO1‐dependent single‐stranded DNA at telomeres activates subsets of DNA damage and spindle checkpoint pathways in budding yeast yku70 delta mutants. Genes Dev 16: 1919‐1933.Google Scholar
  57. McClintock B (1939) The behavior in successive nuclear divisions of a chromosome broken at meiosis. Proc Natl Acad Sci USA 25: 405‐416.Google Scholar
  58. McClintock B (1944) Maize genetics, Carnegie Institution of Washington Year Book. In: Moore JA, ed. Genes, Cells and Organisms. New York: Garland Publishing, Inc. 1987.Google Scholar
  59. Mitton‐Fry RM, Anderson EM, Hughes TR, Lundblad V, Wuttke DS (2002) Conserved structure for single‐stranded telomeric DNA recognition. Science 296: 145‐147.Google Scholar
  60. Munoz‐Jordan JL, Cross GA, de Lange T, Griffith JD (2001) T‐loops at trypanosome telomeres. EMBO J 20: 579‐588.Google Scholar
  61. Murti KG, Prescott DM (1999) Telomeres of polytene chromosomes in a ciliated protozoan terminate in duplex DNA loops. Proc Natl Acad Sci USA 96: 14436‐14439.Google Scholar
  62. Nakamura TM, Cech TR (1998) Reversing time: origin of telomerase. Cell 92: 587‐590.Google Scholar
  63. Oguchi K, Liu H, Tamura K, Takahashi H (1999) Molecular cloning and characterization of AtTERT, a telomerase reverse transcriptase homolog in Arabidopsis thaliana. FEBSLett 457: 465‐469.Google Scholar
  64. Oulton R, Harrington L (2000) Telomeres, telomerase, and cancer: life on the edge of genomic stability. Curr Opin Oncol 12: 74‐81.Google Scholar
  65. Pardue ML, DeBaryshe PG (1999) Telomeres and telomerase: more than the end of the line. Chromosoma 108: 73‐82.Google Scholar
  66. Pennock E, Buckley K, Lundblad V (2001) Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 104: 387‐396.Google Scholar
  67. 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.Google Scholar
  68. Poole AM, Jeffares DC, Pennya D (1998) The path from theRNA world. J Mol Evol 46: 1‐17.Google Scholar
  69. Ray S, Karamysheva Z, Wang L, Shippen DE, Price CM (2002) Interactions between telomerase and primase physically link the telomere and chromosome replication machinery. Mol Cell Biol 22: 5859‐5868.Google Scholar
  70. Regad F, Lebas M, Lescure B (1994) Interstitial telomeric repeats within the Arabidopsis thaliana genome. J Mol Biol 239: 163‐169.Google Scholar
  71. Richards EJ, Ausubel FM (1988) Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell 53: 127‐136.Google Scholar
  72. Riha K, Fajkus J, Siroky J, Vyskot B (1998) Developmental control of telomere lengths and telomerase activity in plants. Plant Cell 10: 1691‐1698.Google Scholar
  73. Riha K, McKnight TD, Fajkus J, Vyskot B, Shippen DE (2000) Analysis of the G‐overhang structures on plant telomeres: evidence for two distinct telomere architectures. Plant J 23: 633‐641.Google Scholar
  74. Riha K, McKnight TD, Griffing LR, Shippen DE (2001) Living with genome instability: plant responses to telomere dysfunction. Science 291: 1797‐1800.Google Scholar
  75. Riha K, Watson JM, Parkey J, Shippen DE (2002) Telomere length deregulation and enhanced sensitivity to genotoxic stress in Arabidopsis mutants deficient in Ku70. EMBO J 21: 2819‐2826.Google Scholar
  76. Shore D (2001) Telomeric chromatin: replicating and wrapping up chromosome ends. Curr Opin Genet Dev 11: 189‐198.Google Scholar
  77. Smogorzewska A, de Lange T (2002) Different telomere damage signaling pathways in human and mouse cells. EMBO J 21: 4338‐4348.Google Scholar
  78. Smogorzewska A, van Steensel B, Bianchi A et al. (2000) Control of human telomere length by TRF1 and TRF2. Mol Cell Biol 20: 1659‐1668.Google Scholar
  79. Smogorzewska A, Karlesder J, Holtgreve‐Grez H, Juach A, de Lange T (2002) DNA ligase IV‐dependent NHEJ of deprotected mammalian telomeres in G1 and G2. Curr. Biol. 12: 1635‐1644.Google Scholar
  80. Stewart SA, Weinberg RA (2000) Telomerase and human tumorigenesis. Semin Cancer Biol 10: 399‐406.Google Scholar
  81. Tamura K, Liu H, Takahashi H (1999) Auxin induction of cell cycle regulated activity of tobacco telomerase. J Biol Chem 274: 20997‐21002.Google Scholar
  82. Tamura K, Adachi Y, Chiba K, Oguchi K, Takahashi H (2002) Identification of Ku70 and Ku80 homologues in Arabidopsis thaliana: evidence for a role in the repair of DNA double‐strand breaks. Plant J 29: 771‐781.Google Scholar
  83. Tremousaygue D, Manevski A, Bardet C, Lescure N, Lescure B (1999) Plant interstitial telomere motifs participate in the control of gene expression in root meristems. Plant J 20: 553‐561.Google Scholar
  84. Weiss H, Scherthan H (2002) Aloe spp.‐plants with vertebrate‐like telomeric sequences. Chromosome Res 10: 155‐164.Google Scholar
  85. Wellinger RJ, Ethier K, Labrecque P, Zakian VA (1996) Evidence for a new step in telomere maintenance. Cell 85: 423‐433.Google Scholar
  86. West CE, Waterworth WM, Story GW, Sunderland PA, Jiang Q, Bray CM (2002) Disruption of the Arabidopsis AtKu80 gene demonstrates an essential role for AtKu80 protein in efficient repair of DNA double‐strand breaks in vivo. Plant J 31: 517‐528.Google Scholar
  87. Yang SW, Jin E, Chung IK, Kim WT (2002) Cell cycle‐dependent regulation of telomerase activity by auxin, abscisic acid and protein phosphorylation in tobacco BY‐2 suspension culture cells. Plant J 29: 617‐626.Google Scholar
  88. Yi X, White DM, Aisner DL, Baur JA, Wright WE, Shay JW (2000) An alternate splicing variant of the human telomerase catalytic subunit inhibits telomerase activity. Neoplasia 2: 433‐440.Google Scholar
  89. Yu EY, Kim SE, Kim JH, Ko JH, Cho MH, Chung IK (2000) Sequence‐specific DNA recognition by the Myb‐like domain of plant telomeric protein RTBP1. J Biol Chem 275: 24208‐24214.Google Scholar
  90. Zentgraf U (1995) Telomere‐binding proteins of Arabidopsis thaliana. Plant Mol Biol 27: 467‐475.Google Scholar
  91. Zentgraf U, Hinderhofer K, Kolb D (2000) Specific association of a small protein with the telomeric DNA‐protein complex during the onset of leaf senescence in Arabidopsis thaliana. Plant Mol Biol 42: 429‐438.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  1. 1.Department of Biochemistry and BiophysicsTexas A&M UniversityCollege StationUSA
  2. 2.Austrian Academy of SciencesGregor Mendel Institute of Molecular Plant BiologyViennaAustria

Personalised recommendations