Invasion of the Arabidopsis genome by the tobacco retrotransposon Tnt1 is controlled by reversible transcriptional gene silencing

Plant Physiology

Volumn 147, Issue 3, 2008, Pages 1264-1278

  Pérez Hormaeche, Javier ^a,b   Potet, Frédérique ^a   Beauclair, Linda ^a   Le Masson, Ivan ^a   Courtial, Béatrice ^a,c   Bouché, Nicolas ^a   Lucas, Hélène ^a  

^a CEMAGREF   (France)

^b INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SEVILLA   (Spain)

^c Laboratoire National de la Protection des Végétaux   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; IVA; NICOTIANA TABACUM;

ARABIDOPSIS PROTEIN; DDM1 PROTEIN, ARABIDOPSIS; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA BINDING PROTEIN; DNA DIRECTED RNA POLYMERASE; MET1 PROTEIN, ARABIDOPSIS; RNA POLYMERASE IV, ARABIDOPSIS; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR;

ADAPTATION; ARABIDOPSIS; ARTICLE; DNA METHYLATION; GENE DOSAGE; GENE SILENCING; GENETICS; LONG TERMINAL REPEAT; METABOLISM; PHYSIOLOGY; PROMOTER REGION; RETROPOSON; TOBACCO;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA-BINDING PROTEINS; DNA-DIRECTED RNA POLYMERASES; GENE DOSAGE; GENE SILENCING; PROMOTER REGIONS (GENETICS); RETROELEMENTS; RNA, SMALL INTERFERING; TERMINAL REPEAT SEQUENCES; TOBACCO; TRANSCRIPTION FACTORS;

EID: 51549119808     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.117846     Document Type: Article

References (65)

1. Andika IB, Kondo H, Rahim MD, Tamada T (2006) Lower levels of transgene silencing in roots is associated with reduced DNA methylation levels at non-symmetrical sites but not at symmetrical sites. Plant Mol Biol 60: 423-435
2. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis. Nature 408: 796-815
3. Bechtold N, Pelletier G (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82: 259-266
4. Bouché N, Lauressergues D, Gasciolli V, Vaucheret H (2006) An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J 25: 3347-3356
5. Casacuberta JM, Grandbastien MA (1993) Characterisation of LTR sequences involved in the protoplast specific expression of the tobacco Tnt1 retrotransposon. Nucleic Acids Res 21: 2087-2093
6. Chaboissier MC, Bucheton A, Finnegan DJ (1998) Copy number control of a transposable element, the I factor, a LINE-like element in Drosophila. Proc Natl Acad Sci USA 95: 11781-11785
7. Chan SW, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis. Nat Rev Genet 6: 351-360
8. Chan SW, Henderson IR, Zhang X, Shah G, Chien JS, Jacobsen SE (2006) RNAi, DRD1, and histone methylation actively target developmentally important non-CG DNA methylation in Arabidopsis. PLoS Genet 2: e83
9. Courtial B, Feuerbach F, Eberhard S, Rohmer L, Chiapello H, Camilleri C, Lucas H (2001) Tnt1 transposition events are induced by in vitro transformation of Arabidopsis, and transposed copies integrate into genes. Mol Genet Genomics 265: 32-42
10. Elmayan T, Balzergue S, Beon F, Bourdon V, Daubremet J, Guenet Y, Mourrain P, Palauqui JC, Vernhettes S, Vialle T, et al (1998) Arabidopsis mutants impaired in cosuppression. Plant Cell 10: 1747-1758
11. Elmayan T, Vaucheret H (1996) Expression of single copies of a strongly expressed 35S transgene can be silenced post-transcriptionally. Plant J 9: 787-797
12. Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, et al (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2: e219
13. Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3: 329-341
14. Feuerbach F, Drouaud J, Lucas H (1997) Retrovirus-like end processing of the tobacco Tnt1 retrotransposon linear intermediates of replication. J Virol 71: 4005-4015
15. Finnegan EJ, Peacock WJ, Dennis ES (1996) Reduced DNA methylation in Arabidopsis results in abnormal plant development. Proc Natl Acad Sci USA 93: 8449-8454
16. Gabriel A, Willems M, Mules EH, Boeke JD (1996) Replication infidelity during a single cycle of Ty1 retrotransposition. Proc Natl Acad Sci USA 93: 7767-7771
17. Gasciolli V, Mallory AC, Bartel DP, Vaucheret H (2005) Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr Biol 15: 1494-1500
18. Gong Z, Morales-Ruiz T, Ariza RR, Roldan-Arjona T, David L, Zhu JK (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111: 803-814
19. Grandbastien MA (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci 3: 181-187
20. Hamilton A, Voinnet O, Chappell L, Baulcombe D (2002) Two classes of short interfering RNA in RNA silencing. EMBO J 21: 4671-4679
21. Herr AJ, Jensen MB, Dalmay T, Baulcombe DC (2005) RNA polymerase IV directs silencing of endogenous DNA. Science 308: 118-120
22. Hirochika H, Okamoto H, Kakutani T (2000) Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12: 357-369
23. Huettel B, Kanno T, Daxinger L, Aufsatz W, Matzke AJ, Matzke M (2006) Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J 25: 2828-2836
24. Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22: 94-97
25. Jones L, Ratcliff F, Baulcombe DC (2001) RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr Biol 11: 747-757
26. Kakutani T (1997) Genetic characterization of late-flowering traits induced by DNA hypomethylation mutation in Arabidopsis. Plant J 12: 1447-1451
27. Kakutani T, Jeddeloh JA, Flowers SK, Munakata K, Richards EJ (1996) Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc Natl Acad Sci USA 93: 12406-12411
28. Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, Riddle NC, Verbsky ML, Richards EJ (2003) Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163: 1109-1122
29. Kanno T, Aufsatz W, Jaligot E, Mette MF, Matzke M, Matzke AJ (2005a) A SNF2-like protein facilitates dynamic control of DNA methylation. EMBO Rep 6: 649-655
30. Kanno T, Huettel B, Mette MF, Aufsatz W, Jaligot E, Daxinger L, Kreil DP, Matzke M, Matzke AJ (2005b) Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet 37: 761-765
31. Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33: 102-106
32. Kato M, Miura A, Bender J, Jacobsen SE, Kakutani T (2003) Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr Biol 13: 421-426
33. Kato M, Takashima K, Kakutani T (2004) Epigenetic control of CACTA transposon mobility in Arabidopsis. Genetics 168: 961-969
34. Lazo GR, Stein PA, Ludwig RA (1991) A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Biotechnology (N Y) 9: 963-967
35. Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, et al (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430: 471-476
36. Lippman Z, May B, Yordan C, Singer T, Martienssen R (2003) Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol 1: E67
37. Lucas H, Feuerbach F, Kunert K, Grandbastien MA, Caboche M (1995) RNA-mediated transposition of the tobacco retrotransposon Tnt1 in Arabidopsis. EMBO J 14: 2364-2373
38. Matzke M, Kanno T, Huettel B, Daxinger L, Matzke JM (2007) Targets of RNA-directed DNA methylation. Curr Opin Plant Biol 10: 512-519
39. Mhiri C, Morel JB, Vernhettes S, Casacuberta JM, Lucas H, Grandbastien MA (1997) The promoter of the tobacco Tnt1 retrotransposon is induced by wounding and by abiotic stress. Plant Mol Biol 33: 257-266
40. Miura A, Kato M, Watanabe K, Kawabe A, Kotani H, Kakutani T (2004) Genomic localization of endogenous mobile CACTA family transposons in natural variants of Arabidopsis. Mol Genet Genomics 270: 524-532
41. Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411: 212-214
42. Moreau-Mhiri C, Morel JB, Audeon C, Ferault M, Grandbastien MA, Lucas H (1996) Regulation of expression of the tobacco Tnt1 retrotransposon in heterologous species following pathogen-related stresses. Plant J 9: 409-419
43. Morel JB, Mourrain P, Beclin C, Vaucheret H (2000) DNA methylation and chromatin structure affect transcriptional and post-transcriptional transgene silencing in Arabidopsis. Curr Biol 10: 1591-1594
44. Morgante M (2006) Plant genome organisation and diversity: the year of the junk! Curr Opin Biotechnol 17: 168-173
45. Okamoto H, Hirochika H (2001) Silencing of transposable elements in plants. Trends Plant Sci 6: 527-534
46. Onodera Y, Haag JR, Ream T, Nunes PC, Pontes O, Pikaard CS (2005) Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120: 613-622
47. Penterman J, Zilberman D, Huh JH, Ballinger T, Henikoff S, Fischer RL (2007) DNA demethylation in the Arabidopsis genome. Proc Natl Acad Sci USA 104: 6752-6757
48. Pontier D, Yahubyan G, Vega D, Bulski A, Saez-Vasquez J, Hakimi MA, Lerbs-Mache S, Colot V, Lagrange T (2005) Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev 19: 2030-2040
49. Pouteau S, Grandbastien MA, Boccara M (1994) Microbial elicitors of plant defense responses activate transcription of a retrotransposon. Plant J 5: 535-542
50. Qi Y, He X, Wang XJ, Kohany O, Jurka J, Hannon GJ (2006) Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443: 1008-1012
51. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis. Genes Dev 20: 3407-3425
52. Saze H, Mittelsten Scheid O, Paszkowski J (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet 34: 65-69
53. Singer T, Yordan C, Martienssen RA (2001) Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev 15: 591-602
54. Smith LM, Pontes O, Searle I, Yelina N, Yousafzai FK, Herr AJ, Pikaard CS, Baulcombe DC (2007) An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19: 1507-1521
55. Sugimoto K, Takeda S, Hirochika H (2000) MYB-related transcription factor NtMYB2 induced by wounding and elicitors is a regulator of the tobacco retrotransposon Tto1 and defense-related genes. Plant Cell 12: 2511-2528
56. Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001-2019
57. Tompa R, McCallum CM, Delrow J, Henikoff JG, van Steensel B, Henikoff S (2002) Genome-wide profiling of DNA methylation reveals transposon targets of CHROMOMETHYLASE3. Curr Biol 12: 65-68
58. Ungerer MC, Strakosh SC, Zhen Y (2006) Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation. Curr Biol 16: R872-R873
59. Vernhettes S, Grandbastien MA, Casacuberta JM (1997) In vivo characterization of transcriptional regulatory sequences involved in the defence-associated expression of the tobacco retrotransposon Tnt1. Plant Mol Biol 35: 673-679
60. Vongs A, Kakutani T, Martienssen RA, Richards EJ (1993) Arabidopsis DNA methylation mutants. Science 260: 1926-1928
61. Walbot V (1992) Reactivation of Mutator transposable elements of maize by ultraviolet light. Mol Gen Genet 234: 353-360
62. Zaratiegui M, Irvine DV, Martienssen RA (2007) Noncoding RNAs and gene silencing. Cell 128: 763-776
63. Zemach A, Li Y, Wayburn B, Ben-Meir H, Kiss V, Avivi Y, Kalchenko V, Jacobsen SE, Grafi G (2005) DDM1 binds Arabidopsis methyl-CpG binding domain proteins and affects their subnuclear localization. Plant Cell 17: 1549-1558
64. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, et al (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126: 1189-1201
65. Zink D, Paro R (1995) Drosophila Polycomb-group regulated chromatin inhibits the accessibility of a trans-activator to its target DNA. EMBO J 14: 5660-5671