Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Science 2 March 2001:
Vol. 291. no. 5509, pp. 1797 - 1800
DOI: 10.1126/science.1057110
Prev | Table of Contents | Next

Reports

Living with Genome Instability: Plant Responses to Telomere Dysfunction

Karel Riha,1 Thomas D. McKnight,2 Lawrence R. Griffing,2 Dorothy E. Shippen1*

Loss of telomere function in metazoans results in catastrophic damage to the genome, cell cycle arrest, and apoptosis. Here we show that the mustard weed Arabidopsis thaliana can survive up to 10 generations without telomerase. The last five generations of telomerase-deficient plants endured increasing levels of cytogenetic damage, which was correlated with developmental anomalies in both vegetative and reproductive organs. Mutants ultimately arrested at a terminal vegetative state harboring shoot meristems that were grossly enlarged, disorganized, and in some cases, dedifferentiated into a callusoid mass. Unexpectedly, late-generation mutants had an extended life-span and remained metabolically active. The differences in plant and animal responses to dysfunctional telomeres may reflect the more plastic nature of plant development and genome organization.

1 Department of Biochemistry and Biophysics, 2128 TAMU, Texas A&M University, College Station, TX 77843-2128, USA.
2 Department of Biology, Texas A&M University, College Station, TX 77843-3258, USA.
*   To whom correspondence should be addressed. E-mail: dshippen{at}tamu.edu

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
STN1 protects chromosome ends in Arabidopsis thaliana.
X. Song, K. Leehy, R. T. Warrington, J. C. Lamb, Y. V. Surovtseva, and D. E. Shippen (2008)
PNAS 105, 19815-19820
   Abstract »    Full Text »    PDF »
Telomeres and Aging.
G. Aubert and P. M. Lansdorp (2008)
Physiol Rev 88, 557-579
   Abstract »    Full Text »    PDF »
Dyskerin Is a Component of the Arabidopsis Telomerase RNP Required for Telomere Maintenance.
K. Kannan, A. D. L. Nelson, and D. E. Shippen (2008)
Mol. Cell. Biol. 28, 2332-2341
   Abstract »    Full Text »    PDF »
ATM regulates the length of individual telomere tracts in Arabidopsis.
L. Vespa, R. T. Warrington, P. Mokros, J. Siroky, and D. E. Shippen (2007)
PNAS 104, 18145-18150
   Abstract »    Full Text »    PDF »
Telomere dynamics and fusion of critically shortened telomeres in plants lacking DNA ligase IV.
M. L. Heacock, R. A. Idol, J. D. Friesner, A. B. Britt, and D. E. Shippen (2007)
Nucleic Acids Res. 35, 6490-6500
   Abstract »    Full Text »    PDF »
Suppression of RICE TELOMERE BINDING PROTEIN1 Results in Severe and Gradual Developmental Defects Accompanied by Genome Instability in Rice.
J.-P. Hong, M. Y. Byun, D.-H. Koo, K. An, J.-W. Bang, I. K. Chung, G. An, and W. T. Kim (2007)
PLANT CELL 19, 1770-1781
   Abstract »    Full Text »    PDF »
Telomere Rapid Deletion Regulates Telomere Length in Arabidopsis thaliana.
J. M. Watson and D. E. Shippen (2007)
Mol. Cell. Biol. 27, 1706-1715
   Abstract »    Full Text »    PDF »
Arabidopsis thaliana telomeric DNA-binding protein 1 is required for telomere length homeostasis and its Myb-extension domain stabilizes plant telomeric DNA binding.
M. G. Hwang and M. H. Cho (2007)
Nucleic Acids Res. 35, 1333-1342
   Abstract »    Full Text »    PDF »
Regulation of Telomerase in Arabidopsis by BT2, an Apparent Target of TELOMERASE ACTIVATOR1.
S. Ren, K. K. Mandadi, A. L. Boedeker, K. S. Rathore, and T. D. McKnight (2007)
PLANT CELL 19, 23-31
   Abstract »    Full Text »    PDF »
Arabidopsis Ribonucleotide Reductases Are Critical for Cell Cycle Progression, DNA Damage Repair, and Plant Development.
C. Wang and Z. Liu (2006)
PLANT CELL 18, 350-365
   Abstract »    Full Text »    PDF »
High incidence of rapid telomere loss in telomerase-deficient Caenorhabditis elegans.
I. Cheung, M. Schertzer, A. Rose, and P. M. Lansdorp (2006)
Nucleic Acids Res. 34, 96-103
   Abstract »    Full Text »    PDF »
ATM and ATR make distinct contributions to chromosome end protection and the maintenance of telomeric DNA in Arabidopsis.
L. Vespa, M. Couvillion, E. Spangler, and D. E. Shippen (2005)
Genes & Dev. 19, 2111-2115
   Abstract »    Full Text »    PDF »
The Arabidopsis Pot1 and Pot2 Proteins Function in Telomere Length Homeostasis and Chromosome End Protection.
E. V. Shakirov, Y. V. Surovtseva, N. Osbun, and D. E. Shippen (2005)
Mol. Cell. Biol. 25, 7725-7733
   Abstract »    Full Text »    PDF »
An increase in telomere sister chromatid exchange in murine embryonic stem cells possessing critically shortened telomeres.
Y. Wang, N. Erdmann, R. J. Giannone, J. Wu, M. Gomez, and Y. Liu (2005)
PNAS 102, 10256-10260
   Abstract »    Full Text »    PDF »
Perturbation of NgTRF1 Expression Induces Apoptosis-Like Cell Death in Tobacco BY-2 Cells and Implicates NgTRF1 in the Control of Telomere Length and Stability.
S. W. Yang, S. K. Kim, and W. T. Kim (2004)
PLANT CELL 16, 3370-3385
   Abstract »    Full Text »    PDF »
TELOMERASE ACTIVATOR1 Induces Telomerase Activity and Potentiates Responses to Auxin in Arabidopsis.
S. Ren, J. S. Johnston, D. E. Shippen, and T. D. McKnight (2004)
PLANT CELL 16, 2910-2922
   Abstract »    Full Text »    PDF »
Phosphorylation of H2AX at Short Telomeres in T Cells and Fibroblasts.
L.-Y. Hao, M. A. Strong, and C. W. Greider (2004)
J. Biol. Chem. 279, 45148-45154
   Abstract »    Full Text »    PDF »
Biochemical properties of Trypanosoma cruzi telomerase.
D. P. Munoz and K. Collins (2004)
Nucleic Acids Res. 32, 5214-5222
   Abstract »    Full Text »    PDF »
Functional links between telomeres and proteins of the DNA-damage response.
F. d'Adda di Fagagna, S.-H. Teo, and S. P. Jackson (2004)
Genes & Dev. 18, 1781-1799
   Abstract »    Full Text »    PDF »
Mre11 Deficiency in Arabidopsis Is Associated with Chromosomal Instability in Somatic Cells and Spo11-Dependent Genome Fragmentation during Meiosis.
J. Puizina, J. Siroky, P. Mokros, D. Schweizer, and K. Riha (2004)
PLANT CELL 16, 1968-1978
   Abstract »    Full Text »    PDF »
Length Regulation and Dynamics of Individual Telomere Tracts in Wild-Type Arabidopsis.
E. V. Shakirov and D. E. Shippen (2004)
PLANT CELL 16, 1959-1967
   Abstract »    Full Text »    PDF »
ATR Regulates a G2-Phase Cell-Cycle Checkpoint in Arabidopsis thaliana.
K. Culligan, A. Tissier, and A. Britt (2004)
PLANT CELL 16, 1091-1104
   Abstract »    Full Text »    PDF »
Distinct dosage requirements for the maintenance of long and short telomeres in mTert heterozygous mice.
N. Erdmann, Y. Liu, and L. Harrington (2004)
PNAS 101, 6080-6085
   Abstract »    Full Text »    PDF »
Plant Telomere Biology.
T. D. McKnight and D. E. Shippen (2004)
PLANT CELL 16, 794-803
   Full Text »    PDF »
The Maize Single myb histone 1 Gene, Smh1, Belongs to a Novel Gene Family and Encodes a Protein That Binds Telomere DNA Repeats in Vitro.
C. O. Marian, S. J. Bordoli, M. Goltz, R. A. Santarella, L. P. Jackson, O. Danilevskaya, M. Beckstette, R. Meeley, and H. W. Bass (2003)
Plant Physiology 133, 1336-1350
   Abstract »    Full Text »    PDF »
Mitotic and Postmitotic Senescence in Plants.
S. Gan (2003)
Sci. Aging Knowl. Environ. 2003, re7-7
   Abstract »    Full Text »    PDF »
Telomere Dysfunction: A Potential Cancer Predisposition Factor.
X. Wu, C. I. Amos, Y. Zhu, H. Zhao, B. H. Grossman, J. W. Shay, S. Luo, W. K. Hong, and M. R. Spitz (2003)
J Natl Cancer Inst 95, 1211-1218
   Abstract »    Full Text »    PDF »
Mutations in Arabidopsis condensin genes disrupt embryogenesis, meristem organization and segregation of homologous chromosomes during meiosis.
N. U. Siddiqui, P. E. Stronghill, R. E. Dengler, C. A. Hasenkampf, and C. D. Riggs (2003)
Development 130, 3283-3295
   Abstract »    Full Text »    PDF »
Expression of the Telomeric Repeat Binding Factor Gene NgTRF1 Is Closely Coordinated with the Cell Division Program in Tobacco BY-2 Suspension Culture Cells.
S. W. Yang, D. H. Kim, J. J. Lee, Y. J. Chun, J.-H. Lee, Y. J. Kim, I. K. Chung, and W. T. Kim (2003)
J. Biol. Chem. 278, 21395-21407
   Abstract »    Full Text »    PDF »
Telomerase Dependence of Telomere Lengthening in ku80 Mutant Arabidopsis.
M. E. Gallego, N. Jalut, and C. I. White (2003)
PLANT CELL 15, 782-789
   Abstract »    Full Text »    PDF »
Ku is required for telomeric C-rich strand maintenance but not for end-to-end chromosome fusions in Arabidopsis.
K. Riha and D. E. Shippen (2003)
PNAS 100, 611-615
   Abstract »    Full Text »    PDF »
Stabilization of Telomere Length and Karyotypic Stability Are Directly Correlated with the Level of hTERT Gene Expression in Primary Fibroblasts.
W. Cui, S. Aslam, J. Fletcher, D. Wylie, M. Clinton, and A. J. Clark (2002)
J. Biol. Chem. 277, 38531-38539
   Abstract »    Full Text »    PDF »
Severe Developmental Defects, Hypersensitivity to DNA-Damaging Agents, and Lengthened Telomeres in Arabidopsis MRE11 Mutants.
P. Bundock and P. Hooykaas (2002)
PLANT CELL 14, 2451-2462
   Abstract »    Full Text »    PDF »
Increased telomere length and hypersensitivity to DNA damaging agents in an Arabidopsis KU70 mutant.
P. Bundock, H. van Attikum, and P. Hooykaas (2002)
Nucleic Acids Res. 30, 3395-3400
   Abstract »    Full Text »    PDF »
Preferential maintenance of critically short telomeres in mammalian cells heterozygous for mTert.
Y. Liu, H. Kha, M. Ungrin, M. O. Robinson, and L. Harrington (2002)
PNAS 99, 3597-3602
   Abstract »    Full Text »    PDF »
How do tumors make ends meet?.
C. Lengauer (2001)
PNAS 98, 12331-12333
   Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)