Genetic architecture of natural variation of telomere length in arabidopsis thaliana

Genetics

Volumn 199, Issue 2, 2014, Pages 625-635

  Fulcher, Nick ^a   Teubenbacher, Astrid ^a   Kerdaffrec, Envel ^a   Farlow, Ashley ^a   Nordborg, Magnus ^a   Riha, Karel ^a,b  

^a GREGOR MENDEL INSTITUTE OF MOLECULAR PLANT BIOLOGY   (Austria)

^b MASARYK UNIVERSITY   (Czech Republic)

Author keywords

Arabidopsis; Centromere mediated genome elimination; Haploid; QTL; Telomere

Indexed keywords

ARABIDOPSIS THALIANA; ARTICLE; CENTROMERE; CHROMOSOME 1; CHROMOSOME 2; FLOW CYTOMETRY; GENE MAPPING; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOME; HAPLOIDY; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; QUANTITATIVE TRAIT LOCUS MAPPING; TELOMERE; TELOMERE HOMEOSTASIS; ARABIDOPSIS; CHROMOSOMAL MAPPING; GENETIC SELECTION; GENETIC VARIATION; GENETICS; MOLECULAR EVOLUTION; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS; CHROMOSOME MAPPING; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENETICS, POPULATION; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; SELECTION, GENETIC; TELOMERE;

EID: 84936777477     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.172163     Document Type: Article

References (69)

1. Alonso-Blanco, C., S. E. D. El-Assal, G. Coupland, and M. Koornneef, 1998a Analysis of natural allelic variation at flowering time loci in the Landsberg erecta and Cape Verde islands ecotypes of Arabidopsis thaliana. Genetics 149: 749–764.
2. Alonso-Blanco, C., A. J. Peeters, M. Koornneef, C. Lister, C. Dean et al., 1998b Development of an AFLP based linkage map of Ler, Col and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/ Cvi recombinant inbred line population. Plant J. 14: 259–271.
3. Andrew, T., A. Aviv, M. Falchi, G. L. Surdulescu, J. P. Gardner et al., 2006 Mapping genetic loci that determine leukocyte telomere length in a large sample of unselected female sibling pairs. Am. J. Hum. Genet. 78: 480–486.
4. Askree, S. H., T. Yehuda, S. Smolikov, R. Gurevich, J. Hawk et al., 2004 A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc. Natl. Acad. Sci. USA 101: 8658–8663.
5. Balasubramanian, S., C. Schwartz, A. Singh, N. Warthmann, M. C. Kim et al., 2009 QTL mapping in new Arabidopsis thaliana advanced intercross-recombinant inbred lines. PLoS ONE 4: e4318.
6. Ben-Ari, G., D. Zenvirth, A. Sherman, L. David, M. Klutstein et al., 2006 Four linked genes participate in controlling sporulation efficiency in budding yeast. PLoS Genet. 2: e195.
7. Blasco, M. A., 2005 Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 6: 611–622.
8. Bodnar, A. G., M. Ouellette, M. Frolkis, S. E. Holt, C. P. Chiu et al., 1998 Extension of life-span by introduction of telomerase into normal human cells. Science 279: 349–352.
9. Broman, K. W., H. Wu, S. Sen, and G. A. Churchill, 2003 R/qtl: QTL mapping in experimental crosses. Bioinformatics 19: 889–890.
10. Brown, A. N., N. Lauter, D. L. Vera, K. A. McLaughlin-Large, T. M. Steele et al., 2011 QTL mapping and candidate gene analysis of telomere length control factors in maize (Zea mays L.). G3 (Bethesda) 1: 437–450.
11. Bryan, T. M., A. Englezou, L. Dalla-Pozza, M. A. Dunham, and R. R. Reddel, 1997 Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat. Med. 3: 1271–1274.
12. Bundock, P., and P. Hooykaas, 2002 Severe developmental defects, hypersensitivity to DNA-damaging agents, and lengthened telomeres in Arabidopsis MRE11 mutants. Plant Cell 14: 2451–2462.
13. Burr, B., F. A. Burr, E. C. Matz, and J. Romeroseverson, 1992 Pinning down loose ends: mapping telomeres and factors affecting their length. Plant Cell 4: 953–960.
14. Cifuentes-Rojas, C., K. Kannan, L. Tseng, and D. E. Shippen, 2011 Two RNA subunits and POT1a are components of Arabidopsis telomerase. Proc. Natl. Acad. Sci. USA 108: 73–78.
15. Cifuentes-Rojas, C., A. D. Nelson, K. A. Boltz, K. Kannan, X. She et al., 2012 An alternative telomerase RNA in Arabidopsis modulates enzyme activity in response to DNA damage. Genes Dev. 26: 2512–2523.
16. Codd, V., M. Mangino, P. van der Harst, P. S. Braund, M. Kaiser et al., 2010 Common variants near TERC are associated with mean telomere length. Nat. Genet. 42: 197–199.
17. Codd, V., C. P. Nelson, E. Albrecht, M. Mangino, J. Deelen et al., 2013 Identification of seven loci affecting mean telomere length and their association with disease. Nat. Genet. 45:422–427, 427e1–2.
18. Cubillos, F. A., E. Billi, E. Zorgo, L. Parts, P. Fargier et al., 2011 Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol. Ecol. 20: 1401–1413.
19. de Lange, T., 2010 How shelterin solves the telomere end-protection problem. Cold Spring Harb. Symp. Quant. Biol. 75: 167–177.
20. Ding, H., M. Schertzer, X. Wu, M. Gertsenstein, S. Selig et al., 2004 Regulation of murine telomere length by Rtel: an essential gene encoding a helicase-like protein. Cell 117: 873–886.
21. Fajkus, J., A. Kovarik, R. Kralovics, and M. Bezdek, 1995 Organization of telomeric and subtelomeric chromatin in the higher plant Nicotiana tabacum. Mol. Gen. Genet. 247: 633–638.
22. Fitzgerald, M. S., K. Riha, F. Gao, S. Ren, T. D. McKnight et al., 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.
23. Gallego, M. E., and C. I. White, 2001 RAD50 function is essential for telomere maintenance in Arabidopsis. Proc. Natl. Acad. Sci. USA 98: 1711–1716.
24. Gallego, M. E., N. Jalut, and C. I. White, 2003 Telomerase dependence of telomere lengthening in Ku80 mutant Arabidopsis. Plant Cell 15: 782–789.
25. Gatbonton, T., M. Imbesi, M. Nelson, J. M. Akey, D. M. Ruderfer et al., 2006 Telomere length as a quantitative trait: genomewide survey and genetic mapping of telomere length-control genes in yeast. PLoS Genet. 2: 907–909.
26. Gohring, J., N. Fulcher, J. Jacak, and K. Riha, 2014 TeloTool: a new tool for telomere length measurement from terminal restriction fragment analysis with improved probe intensity correction. Nucleic Acids Res. 42: e21.
27. Greider, C. W., and E. H. Blackburn, 1985 Identification of a specific telomere terminal transferase-activity in Tetrahymena extracts. Cell 43: 405–413.
28. Heacock, M., E. Spangler, K. Riha, J. Puizina, and D. E. Shippen, 2004 Molecular analysis of telomere fusions in Arabidopsis: multiple pathways for chromosome end-joining. EMBO J. 23: 2304–2313.
29. Kannan, K., A. D. Nelson, and D. E. Shippen, 2008 Dyskerin is a component of the Arabidopsis telomerase RNP required for telomere maintenance. Mol. Cell. Biol. 28: 2332–2341.
30. Keurentjes, J. J. B., L. Bentsink, C. Alonso-Blanco, C. J. Hanhart, H. B. D. Vries et al., 2007 Development of a near-isogenic line population of Arabidopsis thaliana and comparison of mapping power with a recombinant inbred line population. Genetics 175: 891–905.
31. Korte, A., and A. Farlow, 2013 The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9: 29.
32. Kuchar, M., and J. Fajkus, 2004 Interactions of putative telomerebinding proteins in Arabidopsis thaliana: identification of functional TRF2 homolog in plants. FEBS Lett. 578: 311–315.
33. Kwon, C., and I. K. Chung, 2004 Interaction of an Arabidopsis RNA-binding protein with plant single-stranded telomeric DNA modulates telomerase activity. J. Biol. Chem. 279: 12812–12818.
34. Leehy, K. A., J. R. Lee, X. Song, K. B. Renfrew, and D. E. Shippen, 2013 MERISTEM DISORGANIZATION1 encodes TEN1, an essential telomere protein that modulates telomerase processivity in Arabidopsis. Plant Cell 25: 1343–1354.
35. Levy, D., S. L. Neuhausen, S. C. Hunt, M. Kimura, S. J. Hwang et al., 2010 Genome-wide association identifies OBFC1 as a locus involved in human leukocyte telomere biology. Proc. Natl. Acad. Sci. USA 107: 9293–9298.
36. Li, B., and A. J. Lustig, 1996 A novel mechanism for telomere size control in Saccharomyces cerevisiae. Genes Dev. 10: 1310–1326.
37. Liti, G., and E. J. Louis, 2012 Advances in quantitative trait analysis in yeast. PLoS Genet. 8: e1002912.
38. Liti, G., S. Haricharan, F. A. Cubillos, A. L. Tierney, S. Sharp et al., 2009 Segregating YKU80 and TLC1 alleles underlying natural variation in telomere properties in wild yeast. PLoS Genet. 5: e1000659.
39. Long, Q., F. A. Rabanal, D. Meng, C. D. Huber, A. Farlow et al., 2013 Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat. Genet. 45: 884–890.
40. Maillet, G., C. I. White, and M. E. Gallego, 2006 Telomere-length regulation in inter-ecotype crosses of Arabidopsis. Plant Mol. Biol. 62: 859–866.
41. Mangino, M., S. Brouilette, P. Braund, N. Tirmizi, M. Vasa-Nicotera et al., 2008 A regulatory SNP of the BICD1 gene contributes to telomere length variation in humans. Hum. Mol. Genet. 17: 2518–2523.
42. Mangino, M., J. B. Richards, N. Soranzo, G. Zhai, A. Aviv et al., 2009 A genome-wide association study identifies a novel locus on chromosome 18q12.2 influencing white cell telomere length. J. Med. Genet. 46: 451–454.
43. Mangino, M., S. J. Hwang, T. D. Spector, S. C. Hunt, M. Kimura et al., 2012 Genome-wide meta-analysis points to CTC1 and ZNF676 as genes regulating telomere homeostasis in humans. Hum. Mol. Genet. 21: 5385–5394.
44. Marcand, S., V. Brevet, and E. Gilson, 1999 Progressive cis-inhibition of telomerase upon telomere elongation. EMBO J. 18: 3509–3519.
45. Najdekrova, L., and J. Siroky, 2012 NBS1 plays a synergistic role with telomerase in the maintenance of telomeres in Arabidopsis thaliana. BMC Plant Biol. 12: 167.
46. Olovnikov, A. M., 1973 A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J. Theor. Biol. 41: 181–190.
47. R Core Team 2013 R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org/.
48. Ravi, M., and S. W. Chan, 2010 Haploid plants produced by centromere-mediated genome elimination. Nature 464: 615–618.
49. Ren, S., J. S. Johnston, D. E. Shippen, and T. D. McKnight, 2004 TELOMERASE ACTIVATOR1 induces telomerase activity and potentiates responses to auxin in Arabidopsis. Plant Cell 16: 2910–2922.
50. Riha, K., and D. E. Shippen, 2003 Ku is required for telomeric C rich strand maintenance but not for end-to-end chromosome fusions in Arabidopsis. Proc. Natl. Acad. Sci. USA 100: 611–615.
51. Riha, K., T. D. McKnight, L. R. Griffing, and D. E. Shippen, 2001 Living with genome instability: plant responses to telomere dysfunction. Science 291: 1797–1800.
52. Riha, K., J. M. Watson, J. Parkey, and D. E. Shippen, 2002 Telomere length deregulation and enhanced sensitivity to genotoxic stress in Arabidopsis mutants deficient in Ku70. EMBO J. 21: 2819–2826.
53. Rossignol, P., S. Collier, M. Bush, P. Shaw, and J. H. Doonan, 2007 Arabidopsis POT1A interacts with TERT-V(I8), an N-terminal splicing variant of telomerase. J. Cell Sci. 120: 3678–3687.
54. Seymour, D. K., D. L. Filiault, I. M. Henry, J. Monson-Miller, M. Ravi et al., 2012 Rapid creation of Arabidopsis doubled haploid lines for quantitative trait locus mapping. Proc. Natl. Acad. Sci. USA 109: 4227–4232.
55. Shakirov, E. V., and D. E. Shippen, 2004 Length regulation and dynamics of individual telomere tracts in wild-type Arabidopsis. Plant Cell 16: 1959–1967.
56. Shakirov, E. V., Y. V. Surovtseva, N. Osbun, and D. E. Shippen, 2005 The Arabidopsis Pot1 and Pot2 proteins function in telomere length homeostasis and chromosome end protection. Mol. Cell. Biol. 25: 7725–7733.
57. Song, X., K. Leehy, R. T. Warrington, J. C. Lamb, Y. V. Surovtseva et al., 2008 STN1 protects chromosome ends in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 105: 19815–19820.
58. Surovtseva, Y. V., E. V. Shakirov, L. Vespa, N. Osbun, X. Song et al., 2007 Arabidopsis POT1 associates with the telomerase RNP and is required for telomere maintenance. EMBO J. 26: 3653–3661.
59. Surovtseva, Y. V., D. Churikov, K. A. Boltz, X. Song, J. C. Lamb et al., 2009 Conserved telomere maintenance component 1 interacts with STN1 and maintains chromosome ends in higher eukaryotes. Mol. Cell 36: 207–218.
60. Takashi, Y., Y. Kobayashi, K. Tanaka, and K. Tamura, 2009 Arabidopsis replication protein A 70a is required for DNA damage response and telomere length homeostasis. Plant Cell Physiol. 50: 1965–1976.
61. Vannier, J. B., V. Pavicic-Kaltenbrunner, M. I. Petalcorin, H. Ding, and S. J. Boulton, 2012 RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 149: 795–806.
62. Vasa-Nicotera, M., S. Brouilette, M. Mangino, J. R. Thompson, P. Braund et al., 2005 Mapping of a major locus that determines telomere length in humans. Am. J. Hum. Genet. 76: 147–151.
63. Vaughn, L. M., and P. H. Masson, 2011 A QTL study for regions contributing to Arabidopsis thaliana root skewing on tilted surfaces. G3 (Bethesda) 1: 105–115.
64. Wang, S., C. J. Basten, Z. B. Zeng, 2010 Windows QTL Cartographer 2.5 Department of Statistics, North Carolina State University, Raleigh, NC.
65. Watson, J. D., 1972 Origin of concatemeric T7 DNA. Nat. New Biol. 239: 197–201.
66. Watson, J. M., and D. E. Shippen, 2007 Telomere rapid deletion regulates telomere length in Arabidopsis thaliana. Mol. Cell. Biol. 27: 1706–1715.
67. Yoo, H. H., C. Kwon, M. M. Lee, and I. K. Chung, 2007 Singlestranded DNA binding factor AtWHY1 modulates telomere length homeostasis in Arabidopsis. Plant J. 49: 442–451.
68. Zhu, L. X., K. S. Hathcock, P. Hande, P. M. Lansdorp, M. F. Seldin et al., 1998 Telomere length regulation in mice is linked to a novel chromosome locus. Proc. Natl. Acad. Sci. USA 95: 8648–8653.
69. Zhu, Y., V. S. Voruganti, J. Lin, T. Matsuguchi, E. Blackburn et al., 2013 QTL mapping of leukocyte telomere length in American Indians: the Strong Heart Family Study. Aging (Albany, N.Y. Online) 5: 704–716.