Epigenetic regulation of intragenic transposable elements impacts gene transcription in Arabidopsis thaliana

Nucleic Acids Research

Volumn 43, Issue 8, 2015, Pages 3911-3921

  Le, Tu N ^a   Miyazaki, Yuji ^a   Takuno, Shohei ^b   Saze, Hidetoshi ^a  

^a OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; RNA; HETEROCHROMATIN; TRANSPOSON;

ARABIDOPSIS THALIANA; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HOST RESISTANCE; INTRON; NONHUMAN; PLANT GENOME; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSPOSON; ARABIDOPSIS; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HETEROCHROMATIN; METABOLISM;

ARABIDOPSIS THALIANA; EUKARYOTA;

ARABIDOPSIS; DNA METHYLATION; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; HETEROCHROMATIN; INTRONS; TRANSCRIPTION, GENETIC;

EID: 84930216292     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv258     Document Type: Article

References (61)

1. Lander, E.S., Linton, L.M., Birren, B., Nusbaum, C., Zody, M.C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W. et al. (2001) Initial sequencing and analysis of the human genome. Nature, 409, 860-921.
2. Buisine, N., Quesneville, H. and Colot, V. (2008) Improved detection and annotation of transposable elements in sequenced genomes using multiple reference sequence sets. Genomics, 91, 467-475.
3. Schnable, P.S., Ware, D., Fulton, R.S., Stein, J.C., Wei, F., Pasternak, S., Liang, C., Zhang, J., Fulton, L., Graves, T.A. et al. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science, 326, 1112-1115.
4. Cordaux, R. and Batzer, M.A. (2009) The impact of retrotransposons on human genome evolution. Nat. Rev. Genet., 10, 691-703.
5. Lisch, D. (2013) How important are transposons for plant evolution? Nat. Rev. Genet., 14, 49-61.
6. Cowley, M. and Oakey, R.J. (2013) Transposable elements re-wire and fine-tune the transcriptome. PLoS Genet., 9, e1003234.
7. Fedoroff, N.V. (2012) Presidential address. Transposable elements, epigenetics, and genome evolution. Science, 338, 758-767.
8. Lockton, S. and Gaut, B.S. (2009) The contribution of transposable elements to expressed coding sequence in Arabidopsis thaliana. J. Mol. Evol., 68, 80-89.
9. Chen, J.M., Stenson, P.D., Cooper, D.N. and Ferec, C. (2005) A systematic analysis of LINE-1 endonuclease-dependent retrotranspositional events causing human genetic disease. Hum. Genet., 117, 411-427.
10. Callinan, P.A. and Batzer, M.A. (2006) Retrotransposable elements and human disease. Genome Dyn., 1, 104-115.
11. Deininger, P.L. and Batzer, M.A. (1999) Alu repeats and human disease. Mol. Genet. Metab., 67, 183-193.
12. Tsukahara, S., Kobayashi, A., Kawabe, A., Mathieu, O., Miura, A. and Kakutani, T. (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature, 461, 423-426.
13. Mirouze, M., Reinders, J., Bucher, E., Nishimura, T., Schneeberger, K., Ossowski, S., Cao, J., Weigel, D., Paszkowski, J. and Mathieu, O. (2009) Selective epigenetic control of retrotransposition in Arabidopsis. Nature, 461, 427-430.
14. Slotkin, R.K. and Martienssen, R. (2007) Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet., 8, 272-285.
15. Law, J.A. and Jacobsen, S.E. (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet., 11, 204-220.
16. Lisch, D. (2009) Epigenetic regulation of transposable elements in plants. Annu. Rev. Plant Biol., 60, 43-66.
17. Stroud, H., Greenberg, M.V., Feng, S., Bernatavichute, Y.V. and Jacobsen, S.E. (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell, 152, 352-364.
18. Zemach, A., Kim, M.Y., Hsieh, P.H., Coleman-Derr, D., Eshed-Williams, L., Thao, K., Harmer, S.L. and Zilberman, D. (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell, 153, 193-205.
19. Du, J., Zhong, X., Bernatavichute, Y.V., Stroud, H., Feng, S., Caro, E., Vashisht, A.A., Terragni, J., Chin, H.G., Tu, A. et al. (2012) Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell, 151, 167-180.
20. Stroud, H., Do, T., Du, J., Zhong, X., Feng, S., Johnson, L., Patel, D.J. and Jacobsen, S.E. (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat. Struct. Mol. Biol., 21, 64-72.
21. Saze, H., Shiraishi, A., Miura, A. and Kakutani, T. (2008) Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science, 319, 462-465.
22. Hollister, J.D. and Gaut, B.S. (2009) Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res., 19, 1419-1428.
23. Nekrutenko, A. and Li, W.H. (2001) Transposable elements are found in a large number of human protein-coding genes. Trends Genet., 17, 619-621.
24. van de Lagemaat, L.N., Medstrand, P. and Mager, D.L. (2006) Multiple effects govern endogenous retrovirus survival patterns in human gene introns. Genome Biol., 7, R86.
25. Sela, N., Mersch, B., Gal-Mark, N., Lev-Maor, G., Hotz-Wagenblatt, A. and Ast, G. (2007) Comparative analysis of transposed element insertion within human and mouse genomes reveals Alu's unique role in shaping the human transcriptome. Genome Biol., 8, R127.
26. Jiang, S.Y. and Ramachandran, S. (2013) Genome-wide survey and comparative analysis of LTR retrotransposons and their captured genes in rice and sorghum. PLoS One, 8, e71118.
27. Nystedt, B., Street, N.R., Wetterbom, A., Zuccolo, A., Lin, Y.-C., Scofield, D.G., Vezzi, F., Delhomme, N., Giacomello, S., Alexeyenko, A. et al. (2013) The Norway spruce genome sequence and conifer genome evolution. Nature, 497, 579-584.
28. West, P., Li, Q., Ji, L., Eichten, S., Song, J., Vaughn, M.W., Schmitz, R.J. and Springer, N.M. (2014) Genomic distribution of H3K9me2 and DNA methylation in a maize genome. PLoS One, 9, e105267.
29. Saze, H., Kitayama, J., Takashima, K., Miura, S., Harukawa, Y., Ito, T. and Kakutani, T. (2013) Mechanism for full-length RNA processing of Arabidopsis genes containing intragenic heterochromatin. Nat. Commun., 4, 2301.
30. Wang, X., Duan, C.G., Tang, K., Wang, B., Zhang, H., Lei, M., Lu, K., Mangrauthia, S.K., Wang, P., Zhu, G. et al. (2013) RNA-binding protein regulates plant DNA methylation by controlling mRNA processing at the intronic heterochromatin-containing gene IBM1. Proc. Natl. Acad. Sci. U.S.A., 110, 15467-15472.
31. Coustham, V., Vlad, D., Deremetz, A., Gy, I., Cubillos, F.A., Kerdaffrec, E., Loudet, O. and Bouché, N. (2014) SHOOT GROWTH1 Maintains Arabidopsis Epigenomes by Regulating IBM1. PLoS One, 9, e84687.
32. Lei, M., La, H., Lu, K., Wang, P., Miki, D., Ren, Z., Duan, C.-G., Wang, X., Tang, K., Zeng, L. et al. (2014) Arabidopsis EDM2 promotes IBM1 distal polyadenylation and regulates genome DNA methylation patterns. Proc. Natl. Acad. Sci. U.S.A., 111, 527-532.
33. Jurka, J., Kapitonov, V.V., Pavlicek, A., Klonowski, P., Kohany, O. and Walichiewicz, J. (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res., 110, 462-467.
34. Krueger, F. and Andrews, S.R. (2011) Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics, 27, 1571-1572.
35. Akalin, A., Kormaksson, M., Li, S., Garrett-Bakelman, F.E., Figueroa, M.E., Melnick, A. and Mason, C.E. (2012) methylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biol., 13, R87.
36. Blevins, T., Pontvianne, F., Cocklin, R., Podicheti, R., Chandrasekhara, C., Yerneni, S., Braun, C., Lee, B., Rusch, D., Mockaitis, K. et al. (2014) A two-step process for epigenetic inheritance in Arabidopsis. Mol. Cell, 54, 30-42.
37. Trapnell, C., Pachter, L. and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
38. Cao, J., Schneeberger, K., Ossowski, S., Gunther, T., Bender, S., Fitz, J., Koenig, D., Lanz, C., Stegle, O., Lippert, C. et al. (2011)Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet., 43, 956-963.
39. Tajima, F. (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics, 105, 437-460.
40. Nei, M. and Gojobori, T. (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol., 3, 418-426.
41. Vongs, A., Kakutani, T., Martienssen, R.A. and Richards, E.J. (1993) Arabidopsis thaliana DNA methylation mutants. Science, 260, 1926-1928.
42. Bartee, L., Malagnac, F. and Bender, J. (2001) Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev., 15, 1753-1758.
43. Diez, C.M., Roessler, K. and Gaut, B.S. (2014) Epigenetics and plant genome evolution. Curr. Opin. Plant Biol., 18, 1-8.
44. Cokus, S.J., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C.D., Pradhan, S., Nelson, S.F., Pellegrini, M. and Jacobsen, S.E. (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature, 452, 215-219.
45. Lister, R., O'Malley, R.C., Tonti-Filippini, J., Gregory, B.D., Berry, C.C., Millar, A.H. and Ecker, J.R. (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell, 133, 523-536.
46. Rutter, M.T., Cross, K.V. and Van Woert, P.A. (2012) Birth, death and subfunctionalization in the Arabidopsis genome. Trends Plant Sci., 17, 204-212.
47. Yang, L., Takuno, S., Waters, E.R. and Gaut, B.S. (2011) Lowly expressed genes in Arabidopsis thaliana bear the signature of possible pseudogenization by promoter degradation. Mol. Biol. Evol., 28, 1193-1203.
48. Miura, A., Nakamura, M., Inagaki, S., Kobayashi, A., Saze, H. and Kakutani, T. (2009) An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. EMBO J., 28, 1078-1086.
49. Inagaki, S., Miura-Kamio, A., Nakamura, Y., Lu, F., Cui, X., Cao, X., Kimura, H., Saze, H. and Kakutani, T. (2010) Autocatalytic differentiation of epigenetic modifications within the Arabidopsis genome. EMBO J., 29, 3496-3506.
50. Rigal, M., Kevei, Z., Pelissier, T. and Mathieu, O. (2012) DNA methylation in an intron of the IBM1 histone demethylase gene stabilizes chromatin modification patterns. EMBO J., 31, 2981-2993.
51. Tsuchiya, T. and Eulgem, T. (2013) An alternative polyadenylation mechanism coopted to the Arabidopsis RPP7 gene through intronic retrotransposon domestication. Proc. Natl. Acad. Sci. U.S.A., 110, E3535-E3543.
52. Bonardi, V., Tang, S., Stallmann, A., Roberts, M., Cherkis, K. and Dangl, J.L. (2011) Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proc. Natl. Acad. Sci. U.S.A., 108, 16463-16468.
53. Ziolkowski, P.A., Koczyk, G., Galganski, L. and Sadowski, J. (2009) Genome sequence comparison of Col and Ler lines reveals the dynamic nature of Arabidopsis chromosomes. Nucleic Acids Res., 37, 3189-3201.
54. Bennetzen, J.L. and Wang, H. (2014) The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu. Rev. Plant Biol., 65, 505-530.
55. Seymour, D.K., Koenig, D., Hagmann, J., Becker, C. and D, W. (2014) Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization. PLoS Genet., 10, e1004785.
56. Lippman, Z., Gendrel, A.V., Black, M., Vaughn, M.W., Dedhia, N., McCombie, W.R., Lavine, K., Mittal, V., May, B., Kasschau, K.D. et al. (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature, 430, 471-476.
57. Gehring, M., Bubb, K.L. and Henikoff, S. (2009) Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science, 324, 1447-1451.
58. Henderson, I.R. and Jacobsen, S.E. (2008) Tandem repeats upstream of the Arabidopsis endogene SDC recruit non-CG DNA methylation and initiate siRNA spreading. Genes Dev., 22, 1597-1606.
59. Wood, A.J., Schulz, R., Woodfine, K., Koltowska, K., Beechey, C.V., Peters, J., Bourc'his, D. and Oakey, R.J. (2008) Regulation of alternative polyadenylation by genomic imprinting. Genes Dev., 22, 1141-1146.
60. Cowley, M., Wood, A.J., Bohm, S., Schulz, R. and Oakey, R.J. (2012) Epigenetic control of alternative mRNA processing at the imprinted Herc3/Nap1l5 locus. Nucleic Acids Res., 40, 8917-8926.
61. Khan, A.R., Enjalbert, J., Marsollier, A.C., Rousselet, A., Goldringer, I. and Vitte, C. (2013) Vernalization treatment induces site-specific DNA hypermethylation at the VERNALIZATION-A1 (VRN-A1) locus in hexaploid winter wheat. BMC Plant Biol., 13, 209.