Genetic architecture of natural variation of telomere length in Arabidopsis thaliana
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
268962
European Research Council - International
PubMed
25488978
PubMed Central
PMC4317667
DOI
10.1534/genetics.114.172163
PII: genetics.114.172163
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis, QTL, centromere-mediated genome elimination, haploid, telomere,
- MeSH
- Arabidopsis genetika MeSH
- genetická variace * MeSH
- jednonukleotidový polymorfismus MeSH
- lokus kvantitativního znaku MeSH
- mapování chromozomů MeSH
- molekulární evoluce MeSH
- populační genetika MeSH
- selekce (genetika) * MeSH
- telomery * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Telomeres represent the repetitive sequences that cap chromosome ends and are essential for their protection. Telomere length is known to be highly heritable and is derived from a homeostatic balance between telomeric lengthening and shortening activities. Specific loci that form the genetic framework underlying telomere length homeostasis, however, are not well understood. To investigate the extent of natural variation of telomere length in Arabidopsis thaliana, we examined 229 worldwide accessions by terminal restriction fragment analysis. The results showed a wide range of telomere lengths that are specific to individual accessions. To identify loci that are responsible for this variation, we adopted a quantitative trait loci (QTL) mapping approach with multiple recombinant inbred line (RIL) populations. A doubled haploid RIL population was first produced using centromere-mediated genome elimination between accessions with long (Pro-0) and intermediate (Col-0) telomere lengths. Composite interval mapping analysis of this population along with two established RIL populations (Ler-2/Cvi-0 and Est-1/Col-0) revealed a number of shared and unique QTL. QTL detected in the Ler-2/Cvi-0 population were examined using near isogenic lines that confirmed causative regions on chromosomes 1 and 2. In conclusion, this work describes the extent of natural variation of telomere length in A. thaliana, identifies a network of QTL that influence telomere length homeostasis, examines telomere length dynamics in plants with hybrid backgrounds, and shows the effects of two identified regions on telomere length regulation.
Zobrazit více v PubMed
Alonso-Blanco C., El-Assal S. E. D., Coupland G., Koornneef M., 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. PubMed PMC
Alonso-Blanco C., Peeters A. J., Koornneef M., Lister C., Dean C., 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. PubMed
Andrew T., Aviv A., Falchi M., Surdulescu G. L., Gardner J. P., 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. PubMed PMC
Askree S. H., Yehuda T., Smolikov S., Gurevich R., Hawk J., et al. , 2004. A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc. Natl. Acad. Sci. USA 101: 8658–8663. PubMed PMC
Balasubramanian S., Schwartz C., Singh A., Warthmann N., Kim M. C., et al. , 2009. QTL mapping in new Arabidopsis thaliana advanced intercross-recombinant inbred lines. PLoS ONE 4: e4318. PubMed PMC
Ben-Ari G., Zenvirth D., Sherman A., David L., Klutstein M., et al. , 2006. Four linked genes participate in controlling sporulation efficiency in budding yeast. PLoS Genet. 2: e195. PubMed PMC
Blasco M. A., 2005. Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 6: 611–622. PubMed
Bodnar A. G., Ouellette M., Frolkis M., Holt S. E., Chiu C. P., et al. , 1998. Extension of life-span by introduction of telomerase into normal human cells. Science 279: 349–352. PubMed
Broman K. W., Wu H., Sen S., Churchill G. A., 2003. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19: 889–890. PubMed
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. PubMed PMC
Bryan T. M., Englezou A., Dalla-Pozza L., Dunham M. A., Reddel R. R., 1997. Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat. Med. 3: 1271–1274. PubMed
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. PubMed PMC
Burr B., Burr F. A., Matz E. C., Romeroseverson J., 1992. Pinning down loose ends: mapping telomeres and factors affecting their length. Plant Cell 4: 953–960. PubMed PMC
Cifuentes-Rojas C., Kannan K., Tseng L., Shippen D. E., 2011. Two RNA subunits and POT1a are components of Arabidopsis telomerase. Proc. Natl. Acad. Sci. USA 108: 73–78. PubMed PMC
Cifuentes-Rojas C., Nelson A. D., Boltz K. A., Kannan K., She X., et al. , 2012. An alternative telomerase RNA in Arabidopsis modulates enzyme activity in response to DNA damage. Genes Dev. 26: 2512–2523. PubMed PMC
Codd V., Mangino M., van der Harst P., Braund P. S., Kaiser M., et al. , 2010. Common variants near TERC are associated with mean telomere length. Nat. Genet. 42: 197–199. PubMed PMC
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. PubMed PMC
Cubillos F. A., Billi E., Zorgo E., Parts L., Fargier P., et al. , 2011. Assessing the complex architecture of polygenic traits in diverged yeast populations. Mol. Ecol. 20: 1401–1413. PubMed
de Lange T., 2010. How shelterin solves the telomere end-protection problem. Cold Spring Harb. Symp. Quant. Biol. 75: 167–177. PubMed
Ding H., Schertzer M., Wu X., Gertsenstein M., Selig S., et al. , 2004. Regulation of murine telomere length by Rtel: an essential gene encoding a helicase-like protein. Cell 117: 873–886. PubMed
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. PubMed
Fitzgerald M. S., Riha K., Gao F., Ren S., McKnight T. D., 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. PubMed PMC
Gallego M. E., White C. I., 2001. RAD50 function is essential for telomere maintenance in Arabidopsis. Proc. Natl. Acad. Sci. USA 98: 1711–1716. PubMed PMC
Gallego M. E., Jalut N., White C. I., 2003. Telomerase dependence of telomere lengthening in Ku80 mutant Arabidopsis. Plant Cell 15: 782–789. PubMed PMC
Gatbonton T., Imbesi M., Nelson M., Akey J. M., Ruderfer D. M., et al. , 2006. Telomere length as a quantitative trait: genome-wide survey and genetic mapping of telomere length-control genes in yeast. PLoS Genet. 2: 907–909. PubMed PMC
Gohring J., Fulcher N., Jacak J., Riha K., 2014. TeloTool: a new tool for telomere length measurement from terminal restriction fragment analysis with improved probe intensity correction. Nucleic Acids Res. 42.: e21. PubMed PMC
Greider C. W., Blackburn E. H., 1985. Identification of a specific telomere terminal transferase-activity in Tetrahymena extracts. Cell 43: 405–413. PubMed
Heacock M., Spangler E., Riha K., Puizina J., Shippen D. E., 2004. Molecular analysis of telomere fusions in Arabidopsis: multiple pathways for chromosome end-joining. EMBO J. 23: 2304–2313. PubMed PMC
Kannan K., Nelson A. D., Shippen D. E., 2008. Dyskerin is a component of the Arabidopsis telomerase RNP required for telomere maintenance. Mol. Cell. Biol. 28: 2332–2341. PubMed PMC
Keurentjes J. J. B., Bentsink L., Alonso-Blanco C., Hanhart C. J., Vries H. B. D., 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. PubMed PMC
Korte A., Farlow A., 2013. The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9: 29. PubMed PMC
Kuchar M., Fajkus J., 2004. Interactions of putative telomere-binding proteins in Arabidopsis thaliana: identification of functional TRF2 homolog in plants. FEBS Lett. 578: 311–315. PubMed
Kwon C., Chung I. K., 2004. Interaction of an Arabidopsis RNA-binding protein with plant single-stranded telomeric DNA modulates telomerase activity. J. Biol. Chem. 279: 12812–12818. PubMed
Leehy K. A., Lee J. R., Song X., Renfrew K. B., Shippen D. E., 2013. MERISTEM DISORGANIZATION1 encodes TEN1, an essential telomere protein that modulates telomerase processivity in Arabidopsis. Plant Cell 25: 1343–1354. PubMed PMC
Levy D., Neuhausen S. L., Hunt S. C., Kimura M., Hwang S. J., 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. PubMed PMC
Li B., Lustig A. J., 1996. A novel mechanism for telomere size control in Saccharomyces cerevisiae. Genes Dev. 10: 1310–1326. PubMed
Liti G., Louis E. J., 2012. Advances in quantitative trait analysis in yeast. PLoS Genet. 8: e1002912. PubMed PMC
Liti G., Haricharan S., Cubillos F. A., Tierney A. L., Sharp S., et al. , 2009. Segregating YKU80 and TLC1 alleles underlying natural variation in telomere properties in wild yeast. PLoS Genet. 5: e1000659. PubMed PMC
Long Q., Rabanal F. A., Meng D., Huber C. D., Farlow A., et al. , 2013. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat. Genet. 45: 884–890. PubMed PMC
Maillet G., White C. I., Gallego M. E., 2006. Telomere-length regulation in inter-ecotype crosses of Arabidopsis. Plant Mol. Biol. 62: 859–866. PubMed
Mangino M., Brouilette S., Braund P., Tirmizi N., Vasa-Nicotera M., et al. , 2008. A regulatory SNP of the BICD1 gene contributes to telomere length variation in humans. Hum. Mol. Genet. 17: 2518–2523. PubMed
Mangino M., Richards J. B., Soranzo N., Zhai G., Aviv A., 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. PubMed PMC
Mangino M., Hwang S. J., Spector T. D., Hunt S. C., Kimura M., 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. PubMed PMC
Marcand S., Brevet V., Gilson E., 1999. Progressive cis-inhibition of telomerase upon telomere elongation. EMBO J. 18: 3509–3519. PubMed PMC
Najdekrova L., Siroky J., 2012. NBS1 plays a synergistic role with telomerase in the maintenance of telomeres in Arabidopsis thaliana. BMC Plant Biol. 12: 167. PubMed PMC
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. PubMed
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/.
Ravi M., Chan S. W., 2010. Haploid plants produced by centromere-mediated genome elimination. Nature 464: 615–618. PubMed
Ren S., Johnston J. S., Shippen D. E., McKnight T. D., 2004. TELOMERASE ACTIVATOR1 induces telomerase activity and potentiates responses to auxin in Arabidopsis. Plant Cell 16: 2910–2922. PubMed PMC
Riha K., Shippen D. E., 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. PubMed PMC
Riha K., McKnight T. D., Griffing L. R., Shippen D. E., 2001. Living with genome instability: plant responses to telomere dysfunction. Science 291: 1797–1800. PubMed
Riha K., Watson J. M., Parkey J., Shippen D. E., 2002. Telomere length deregulation and enhanced sensitivity to genotoxic stress in Arabidopsis mutants deficient in Ku70. EMBO J. 21: 2819–2826. PubMed PMC
Rossignol P., Collier S., Bush M., Shaw P., Doonan J. H., 2007. Arabidopsis POT1A interacts with TERT-V(I8), an N-terminal splicing variant of telomerase. J. Cell Sci. 120: 3678–3687. PubMed
Seymour D. K., Filiault D. L., Henry I. M., Monson-Miller J., Ravi M., et al. , 2012. Rapid creation of Arabidopsis doubled haploid lines for quantitative trait locus mapping. Proc. Natl. Acad. Sci. USA 109: 4227–4232. PubMed PMC
Shakirov E. V., Shippen D. E., 2004. Length regulation and dynamics of individual telomere tracts in wild-type Arabidopsis. Plant Cell 16: 1959–1967. PubMed PMC
Shakirov E. V., Surovtseva Y. V., Osbun N., Shippen D. E., 2005. The Arabidopsis Pot1 and Pot2 proteins function in telomere length homeostasis and chromosome end protection. Mol. Cell. Biol. 25: 7725–7733. PubMed PMC
Song X., Leehy K., Warrington R. T., Lamb J. C., Surovtseva Y. V., et al. , 2008. STN1 protects chromosome ends in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 105: 19815–19820. PubMed PMC
Surovtseva Y. V., Shakirov E. V., Vespa L., Osbun N., Song X., et al. , 2007. Arabidopsis POT1 associates with the telomerase RNP and is required for telomere maintenance. EMBO J. 26: 3653–3661. PubMed PMC
Surovtseva Y. V., Churikov D., Boltz K. A., Song X., Lamb J. C., et al. , 2009. Conserved telomere maintenance component 1 interacts with STN1 and maintains chromosome ends in higher eukaryotes. Mol. Cell 36: 207–218. PubMed PMC
Takashi Y., Kobayashi Y., Tanaka K., Tamura K., 2009. Arabidopsis replication protein A 70a is required for DNA damage response and telomere length homeostasis. Plant Cell Physiol. 50: 1965–1976. PubMed
Vannier J. B., Pavicic-Kaltenbrunner V., Petalcorin M. I., Ding H., Boulton S. J., 2012. RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 149: 795–806. PubMed
Vasa-Nicotera M., Brouilette S., Mangino M., Thompson J. R., Braund P., et al. , 2005. Mapping of a major locus that determines telomere length in humans. Am. J. Hum. Genet. 76: 147–151. PubMed PMC
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. PubMed PMC
Wang, S., C. J. Basten, Z. B. Zeng, 2010 Windows QTL Cartographer 2.5 Department of Statistics, North Carolina State University, Raleigh, NC.
Watson J. D., 1972. Origin of concatemeric T7 DNA. Nat. New Biol. 239: 197–201. PubMed
Watson J. M., Shippen D. E., 2007. Telomere rapid deletion regulates telomere length in Arabidopsis thaliana. Mol. Cell. Biol. 27: 1706–1715. PubMed PMC
Yoo H. H., Kwon C., Lee M. M., Chung I. K., 2007. Single-stranded DNA binding factor AtWHY1 modulates telomere length homeostasis in Arabidopsis. Plant J. 49: 442–451. PubMed
Zhu L. X., Hathcock K. S., Hande P., Lansdorp P. M., Seldin M. F., et al. , 1998. Telomere length regulation in mice is linked to a novel chromosome locus. Proc. Natl. Acad. Sci. USA 95: 8648–8653. PubMed PMC
Zhu Y., Voruganti V. S., Lin J., Matsuguchi T., Blackburn E., 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. PubMed PMC
Molecular characterization of Chlamydomonas reinhardtii telomeres and telomerase mutants