Telomere dynamics in the lower plant Physcomitrella patens

Plant Molecular Biology

Volumn 87, Issue 6, 2015, Pages 591-601

  Fojtová, Miloslava ^a,b   Sýkorová, Eva ^a,b   Najdekrová, Lucie ^a   Polanská, Pavla ^a   Zachová, Dagmar ^a   Vagnerová, Radka ^c   Angelis, Karel J ^c   Fajkus, Jiří ^a,b  

^a MASARYK UNIVERSITY   (Czech Republic)

^b INSTITUTE OF BIOPHYSICS   (Czech Republic)

^c INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

Author keywords

DSB repair mutants; Physcomitrella patens; PpTERT structure; Telomerase; Telomere maintenance

Indexed keywords

PLANT DNA; TELOMERASE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; BRYOPSIDA; DNA REPAIR; DNA SEQUENCE; DOUBLE STRANDED DNA BREAK; GENETICS; HOMOLOGOUS RECOMBINATION; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PLANT CHROMOSOME; SEQUENCE ALIGNMENT; TELOMERE; TELOMERE HOMEOSTASIS;

AMINO ACID SEQUENCE; ARABIDOPSIS; BASE SEQUENCE; BRYOPSIDA; CHROMOSOMES, PLANT; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA, PLANT; HOMOLOGOUS RECOMBINATION; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PHYLOGENY; PLANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TELOMERASE; TELOMERE; TELOMERE HOMEOSTASIS;

EID: 84930704160     PISSN: 01674412     EISSN: 15735028     Source Type: Journal    
DOI: 10.1007/s11103-015-0299-9     Document Type: Article

References (67)

1. Akimcheva S, Zellinger B, Riha K (2008) Genome stability in Arabidopsis cells exhibiting alternative lengthening of telomeres. Cytogenet Genome Res 122:388–395. doi:10.1159/000167827
2. Albert VA et al (2013) The Amborella genome and the evolution of flowering plants. Science 342:1467. doi:10.1126/science.1241089
3. Amiard S, Charbonnel C, Allain E, Depeiges A, White CI, Gallego ME (2010) Distinct roles of the ATR kinase and the Mre11-Rad50-Nbs1 complex in the maintenance of chromosomal stability in Arabidopsis. Plant Cell 22:3020–3033. doi:10.1105/tpc.110.078527
4. Amiard S, White C, Gallego ME (2011) Recombination proteins and telomere stability in plants. Curr Protein Pept Sci 12:84–92
5. Aya K, Kobayashi M, Tanaka J, Ohyanagi H, Suzuki T, Yano K, Takano T, Yano K, Matsuoka M (2015) De novo transcriptome assembly of a fern, Lygodium japonicum, and a web resource database, Ljtrans DB. Plant Cell Physiol 56:e5. doi:10.1093/pcp/pcu184
6. Banks JA, Nishiyama T, Hasebe M et al (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332:960–963. doi:10.1126/science.1203810
7. Benkova E, Ivanchenko MG, Friml J, Shishkova S, Dubrovsky JG (2009) A morphogenetic trigger: is there an emerging concept in plant developmental biology? Trends Plant Sci 14:189–193. doi:10.1016/j.tplants.2009.01.006
8. 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. doi:10.1105/Tpc.005959
9. Charbonnel C, Gallego ME, White CI (2010) Xrcc1-dependent and Ku-dependent DNA double-strand break repair kinetics in Arabidopsis plants. Plant J 64:280–290. doi:10.1111/j.1365-313X.2010.04331.x
10. Charbonnel C, Allain E, Gallego ME, White CI (2011) Kinetic analysis of DNA double-strand break repair pathways in Arabidopsis. DNA Repair (Amst) 10:611–619. doi:10.1016/j.dnarep.2011.04.002
11. de Lange T (2009) How telomeres solve the end-protection problem. Science 326:948–952. doi:10.1126/science.1170633
12. Dellaporta SL, Wood J, Hicks JB (1983) A Plant DNA minipreparation. Version II. Plant Mol Biol Rep 1:19–21
13. Draskovic I, Arnoult N, Steiner V, Bacchetti S, Lomonte P, Londono-Vallejo A (2009) Probing PML body function in ALT cells reveals spatiotemporal requirements for telomere recombination. Proc Natl Acad Sci U S A 106:15726–15731. doi:10.1073/pnas.0907689106
14. 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. doi:10.1007/Bf00290355
15. Fajkus J, Kovarik A, Kralovics R (1996) Telomerase activity in plant cells. FEBS Lett 391:307–309
16. Fajkus J, Fulneckova J, Hulanova M, Berkova K, Riha K, Matyasek R (1998) Plant cells express telomerase activity upon transfer to callus culture, without extensively changing telomere lengths. Mol Gen Genet 260:470–474
17. Fajkus J, Sykorova E, Leitch AR (2005) Telomeres in evolution and evolution of telomeres. Chromosome Res 13:469–479. doi:10.1007/s10577-005-0997-2
18. Fitzgerald MS, McKnight TD, Shippen DE (1996) Characterization and developmental patterns of telomerase expression in plants. Proc Natl Acad Sci U S A 93:14422–14427
19. Friml J, Benfey P, Benkova E et al (2006) Apical-basal polarity: why plant cells don’t stand on their heads. Trends Plant Sci 11:12–14. doi:10.1016/j.tpnats.2005.11.010
20. Fulneckova J, Hasikova T, Fajkus J, Lukesova A, Elias M, Sykorova E (2012) Dynamic evolution of telomeric sequences in the green algal order Chlamydomonadales. Genome Biol Evol 4:248–264. doi:10.1093/gbe/evs007
21. Fulneckova J, Sevcikova T, Fajkus J, Lukesova A, Lukes M, Vlcek C, Lang BF, King E, Elias M, Sykorova E (2013) A broad phylogenetic survey unveils the diversity and evolution of telomeres in eukaryotes. Genome Biol Evol 5:468–483. doi:10.1093/Gbe/Evt019
22. Gallego ME, White CI (2001) RAD50 function is essential for telomere maintenance in Arabidopsis. Proc Natl Acad Sci U S A 98:1711–1716. doi:10.1073/pnas.98.4.1711
23. Gallego ME, Bleuyard JY, Daoudal-Cotterell S, Jallut N, White CI (2003) Ku80 plays a role in non-homologous recombination but is not required for T-DNA integration in Arabidopsis. Plant J 35:557–565
24. Graham LE, Cook ME, Busse JS (2000) The origin of plants: body plan changes contributing to a major evolutionary radiation. Proc Natl Acad Sci U S A 97:4535–4540. doi:10.1073/pnas.97.9.4535
25. Greider CW, Blackburn EH (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43:405–413. doi:10.1016/0092-8674(85)90170-9
26. Greider CW, Blackburn EH (1987) The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with 2 kinds of primer specificity. Cell 51:887–898. doi:10.1016/0092-8674(87)90576-9
27. Greider CW, Blackburn EH (1989) A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337:331–337. doi:10.1038/337331a0
28. Harries PA, Pan AH, Quatrano RS (2005) Actin-related protein2/3 complex component ARPC1 is required for proper cell morphogenesis and polarized cell growth in Physcomitrella patens. Plant Cell 17:2327–2339. doi:10.1105/tpc.105.033266
29. Heacock ML, Idol RA, Friesner JD, Britt AB, Shippen DE (2007) Telomere dynamics and fusion of critically shortened telomeres in plants lacking DNA ligase IV. Nucleic Acids Res 35:6490–6500. doi:10.1093/nar/gkm472
30. Herbert BS, Hochreiter AE, Wright WE, Shay JW (2006) Nonradioactive detection of telomerase activity using the telomeric repeat amplification protocol. Nat Protoc 1:1583–1590. doi:10.1038/nprot.2006.239
31. Hola M, Kozak J, Vagnerova R, Angelis KJ (2013) Genotoxin induced mutagenesis in the model plant Physcomitrella patens. Biomed Res Int 2013:535049. doi:10.1155/2013/535049
32. Ijdo JW, Wells RA, Baldini A, Reeders ST (1991) Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res 19:4780. doi:10.1093/nar/19.17.4780
33. Jaske K, Mokros P, Mozgova I, Fojtova M, Fajkus J (2013) A telomerase-independent component of telomere loss in chromatin assembly factor 1 mutants of Arabidopsis thaliana. Chromosoma 122:285–293. doi:10.1007/s00412-013-0400-6
34. Kamisugi Y, Schlink K, Rensing SA, Schween G, von Stackelberg M, Cuming AC, Reski R, Cove DJ (2006) The mechanism of gene targeting in Physcomitrella patens: homologous recombination, concatenation and multiple integration. Nucleic Acids Res 34:6205–6214
35. Kamisugi Y, Schaefer DG, Kozak J, Charlot F, Vrielynck N, Holá M, Angelis KJ, Cuming AC, Nogue F (2012) MRE11 and RAD50, but not NBS1, are essential for gene targeting in the moss Physcomitrella patens. Nucleic Acids Res 40:3496–3510. doi:10.1093/nar/gkr1272
36. Kazda A, Zellinger B, Rossler M, Derboven E, Kusenda B, Riha K (2012) Chromosome end protection by blunt-ended telomeres. Genes Dev 26:1703–1713. doi:10.1101/gad.194944.112
37. Knight CD, Cove DJ, Cuming AC, Quatrano RS (2002) Moss gene technology. In: Gilmartin PM, Bowler C (eds) Molecular plant biology, vol 2. Oxford University Press, Oxford, pp 285–299
38. Kozak J, West CE, White C, da Costa-Nunes JA, Angelis KJ (2009) Rapid repair of DNA double strand breaks in Arabidopsis thaliana is dependent on proteins involved in chromosome structure maintenance. DNA Repair (Amst) 8:413–419. doi:10.1016/j.dnarep.2008.11.012
39. Majerska J, Sykorova E, Fajkus J (2011) Non-telomeric activities of telomerase. Mol BioSyst 7:1013–1023. doi:10.1039/C0mb00268b
40. McClintock B (1941) The stability of broken rnds of chromosomes in Zea mays. Genetics 26:234–282
41. Ming R, VanBuren R, Liu Y et al (2013) Genome of the long-living sacred lotus (Nelumbo nucifera Gaertn.). Genome Biol 14:R41. doi:10.1186/Gb-2013-14-5-R41
42. 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. doi:10.1186/1471-2229-12-167
43. Olive PL, Banath JP (2006) The comet assay: a method to measure DNA damage in individual cells. Nat Protoc 1:23–29. doi:10.1038/nprot.2006.5
44. Olovnikov AM (1971) Principle of marginotomy in template synthesis of polynucleotides. Dokl Akad Nauk SSSR 201:1496–1499
45. Pfaffl MW (2004) Quantification strategies in real-time PCR. In: Bustin SA (ed) A-Z of quantitative PCR. International University Line, La Jolla, pp 87–112
46. 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. doi:10.1007/Bf02254961
47. Prigge MJ, Bezanilla M (2010) Evolutionary crossroads in developmental biology: Physcomitrella patens. Development 137:3535–3543. doi:10.1242/Dev.049023
48. Rensing SA, Fritzowsky D, Lang D, Reski R (2005) Protein encoding genes in an ancient plant: analysis of codon usage, retained genes and splice sites in a moss, Physcomitrella patens. BMC Genom 6:43. doi:10.1186/1471-2164-6-43
49. Rensing SA, Lang D, Zimmer AD et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69. doi:10.1126/science.1150646
50. Riha K, Fajkus J, Siroky J, Vyskot B (1998) Developmental control of telomere lengths and telomerase activity in plants. Plant Cell 10:1691–1698
51. 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. doi:10.1093/emboj/21.11.2819
52. Rossignol P, Collier S, Bush M, Shaw P, Doonan JH (2007) Arabidopsis POT1A interacts with TERT-V(I8), an N-terminal splicing variant of telomerase. J Cell Sci 120:3678–3687. doi:10.1242/jcs.004119
53. Ruckova E, Friml J, Schrumpfova PP, Fajkus J (2008) Role of alternative telomere lengthening unmasked in telomerase knock-out mutant plants. Plant Mol Biol 66:637–646. doi:10.1007/s11103-008-9295-7
54. Schaefer DG (2002) A new moss genetics: targeted mutagenesis in Physcomitrella patens. Annu Rev Plant Biol 53:477–501. doi:10.1146/annurev.arplant.53.100301.135202
55. Shakirov EV, Perroud PF, Nelson AD, Cannell ME, Quatrano RS, Shippen DE (2010) Protection of Telomeres 1 is required for telomere integrity in the moss Physcomitrella patens. Plant Cell 22:1838–1848. doi:10.1105/tpc.110.075846
56. Smidkova M, Hola M, Angelis KJ (2010) Efficient biolistic transformation of the moss Physcomitrella patens. Biol Plant 54:777–780
57. Suzuki K (2004) Characterization of telomere DNA among five species of pteridophytes and bryophytes. J Bryol 26:175–180. doi:10.1179/037366804x5279
58. Sykorova E, Fajkus J (2009) Structure-function relationships in telomerase genes. Biol Cell 101:375–392. doi:10.1042/Bc20080205
59. Sykorova E, Lim KY, Chase MW, Knapp S, Leitch IJ, Leitch AR, Fajkus J (2003a) The absence of Arabidopsis-type telomeres in Cestrum and closely related genera Vestia and Sessea (Solanaceae): first evidence from eudicots. Plant J 34:283–291
60. Sykorova E, Lim KY, Kunicka Z, Chase MW, Bennett MD, Fajkus J, Leitch AR (2003b) Telomere variability in the monocotyledonous plant order Asparagales. Proc Biol Sci 270:1893–1904. doi:10.1098/rspb.2003.2446
61. Sykorova E, Fajkus J, Meznikova M, Lim KY, Neplechova K, Blattner FR, Chase MW, Leitch A (2006a) Minisatellite telomeres occur in the family Alliaceae but are lost in Allium. Am J Bot 93:814–823
62. Sykorova E, Rowland A, Leitch AR, Fajkus J (2006b) Asparagales telomerases which synthesize the human type of telomeres. Plant Mol Biol 60:633–646. doi:10.1007/s11103-005-5091-9
63. Sykorova E, Fulneckova J, Mokros P, Fajkus J, Fojtova M, Peska V (2012) Three TERT genes in Nicotiana tabacum. Chromosome Res 20:381–394. doi:10.1007/s10577-012-9282-3
64. Viaene T, Landberg K, Thelander M, Medvecka E, Pederson E, Feraru E, Cooper ED, Karimi M, Delwiche CF, Ljung K, Geisler M, Sundberg E, Friml J (2014) Directional auxin transport mechanisms in early diverging land plants. Curr Biol 24:2786–2791. doi:10.1016/j.cub.2014.09.056
65. Worden AZ, Lee JH, Mock T et al (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268–272. doi:10.1126/science.1167222
66. Zachova D, Fojtova M, Dvorackova M, Mozgova I, Lermontova I, Peska V, Schubert I, Fajkus J, Sykorova E (2013) Structure-function relationships during transgenic telomerase expression in Arabidopsis. Physiol Plant 149:114–126. doi:10.1111/Ppl.12021
67. Zimmer AD, Lang D, Buchta K, Rombauts S, Nishiyama T, Hasebe M, van de Peer Y, Rensing SA, Reski R (2013) Reannotation and extended community resources for the genome of the non-seed plant Physcomitrella patens provide insights into the evolution of plant gene structures and functions. BMC Genom 14:498. doi:10.1186/1471-2164-14-498