Extensive amplification of the E2F transcription factor binding sites by transposons during evolution of Brassica species

Plant Journal

Volumn 77, Issue 6, 2014, Pages 852-862

  Hénaff, Elizabeth ^a   Vives, Cristina ^a   Desvoyes, Bénédicte ^b   Chaurasia, Ankita ^a   Payet, Jordi ^c   Gutierrez, Crisanto ^b   Casacuberta, Josep M ^a  

^a CENTRE FOR RESEARCH IN AGRICULTURAL GENOMICS CRAG   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c NONE   (Spain)

Author keywords

Arabidopsis lyrata; Arabidopsis thaliana; Brassica rapa; Capsela rubella; evolution; MITE; Thelungella halopila; transcription factor binding site; transcriptional network; transposon

Indexed keywords

BINDING SITES; TRANSCRIPTION FACTORS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICA RAPA; CAPSELA RUBELLA; EVOLUTION; MITE; THELUNGELLA HALOPILA; TRANSCRIPTION FACTOR BINDING SITES; TRANSCRIPTIONAL NETWORKS; TRANSPOSON;

GENES;

TRANSCRIPTION FACTOR BINDING SITE; TRANSCRIPTION FACTOR E2F; VEGETABLE PROTEIN;

ARABIDOPSIS LYRATA; ARABIDOPSIS THALIANA; ARTICLE; BINDING SITE; BRASSICA; BRASSICA RAPA; CAPSELA RUBELLA; EVOLUTION; GENE AMPLIFICATION; GENE EXPRESSION REGULATION; GENETICS; INVERTED REPEAT; MITE; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT GENOME; PROMOTER REGION; SPECIES DIFFERENTIATION; THELUNGELLA HALOPILA; TRANSCRIPTIONAL NETWORK; TRANSPOSON;

ARABIDOPSIS LYRATA; ARABIDOPSIS THALIANA; BRASSICA RAPA; CAPSELA RUBELLA; EVOLUTION; MITE; THELUNGELLA HALOPILA; TRANSCRIPTION FACTOR BINDING SITE; TRANSCRIPTIONAL NETWORK; TRANSPOSON;

BASE SEQUENCE; BINDING SITES; BRASSICA; DNA TRANSPOSABLE ELEMENTS; E2F TRANSCRIPTION FACTORS; EVOLUTION, MOLECULAR; GENE AMPLIFICATION; GENE EXPRESSION REGULATION, PLANT; GENETIC SPECIATION; GENOME, PLANT; INVERTED REPEAT SEQUENCES; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PROMOTER REGIONS, GENETIC;

EID: 84896743900     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12434     Document Type: Article

References (42)

1. Ahmed, I., Sarazin, A., Bowler, C., Colot, V., and, Quesneville, H., (2011) Genome-wide evidence for local DNA methylation spreading from small RNA-targeted sequences in Arabidopsis. Nucleic Acids Res. 39, 6919-6931.
2. Beilstein, M., Nagalingum, N., Clements, M., Manchester, S., and, Mathews, S., (2010) Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 107, 18724-18728.
3. Benson, G., (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573-580.
4. Bourque, G., (2009) Transposable elements in gene regulation and in the evolution of vertebrate genomes. Curr. Opin. Genet. Dev. 19, 607-612.
5. Bourque, G., Leong, B., Vega, V.B., et al. (2008) Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res. 18, 1752-1762.
6. Bowler, C., Benvenuto, G., Laflamme, P., Molino, D., Probst, A.V., Tariq, M., and, Paszkowski, J., (2004) Chromatin techniques for plant cells. Plant J. 39, 776-789.
7. Bucher, E., Reinders, J., and, Mirouze, M., (2012) Epigenetic control of transposon transcription and mobility in Arabidopsis. Curr. Opin. Plant Biol. 15, 503-510.
8. Cowley, M., and, Oakey, R.J., (2013) Transposable elements re-wire and fine-tune the transcriptome. PLoS Genet. 9, e1003234.
9. De Veylder, L., Beeckman, T., Beemster, G.T., et al. (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J. 21, 1360-1368.
10. DeGregori, J., and, Johnson, D.G., (2006) Distinct and overlapping roles for E2F family members in transcription, proliferation and apoptosis. Curr. Mol. Med. 6, 739-748.
11. Feschotte, C., (2008) Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9, 397-405.
12. Garcia-Mas, J., Benjak, A., Sanseverino, W., et al. (2012) The genome of melon (Cucumis melo L.). Proc. Natl Acad. Sci. USA, 109, 11872-11877.
13. Guermonprez, H., Hénaff, E., Cifuentes, M., and, Casacuberta, J., (2012) MITEs, miniature elements with a major role in plant genome evolution. In Topics in Current Genetics: Plant Transposable Elements (, Grandbastien, M.A., and, Casacuberta, J.M.,eds). Heidelberg/Berlin: Springer-Verlag, pp. 112-124.
14. van den Heuvel, S., and, Dyson, N.J., (2008) Conserved functions of the pRB and E2F families. Nat. Rev. Mol. Cell Biol. 9, 713-724.
15. Heyman, J., Van den Daele, H., De Wit, K., Boudolf, V., Berckmans, B., Verkest, A., Alvim Kamei, C.L., De Jaeger, G., Koncz, C., and, De Veylder, L., (2011) Arabidopsis ULTRAVIOLET-B-INSENSITIVE4 maintains cell division activity by temporal inhibition of the anaphase-promoting complex/cyclosome. Plant Cell, 23, 4394-4410.
16. Hu, T.T., Pattyn, P., Bakker, E.G., et al. (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat. Genet. 43, 476-481.
17. Jacob, Y., Feng, S., LeBlanc, C.A., Bernatavichute, Y.V., Stroud, H., Cokus, S., Johnson, L.M., Pellegrini, M., Jacobsen, S.E., and, Michaels, S.D., (2009) ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing. Nat. Struct. Mol. Biol. 16, 763-768.
18. Jacques, P.-E., Jeyakani, J., and, Bourque, G., (2013) The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet. 9, e1003504.
19. Kaul, S., Koo, H.L., Jenkins, J., et al. (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796-815.
20. Kunarso, G., Chia, N.Y., Jeyakani, J., Hwang, C., Lu, X.Y., Chan, Y.S., Ng, H.H., and, Bourque, G., (2010) Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 42, 631-634.
21. Lammens, T., Li, J., Leone, G., and, De Veylder, L., (2009) Atypical E2Fs: new players in the E2F transcription factor family. Trends Cell Biol. 19, 111-118.
22. Lisch, D., (2013) How important are transposons for plant evolution? Nat. Rev. Genet. 14, 49-61.
23. Luo, C., Sidote, D.J., Zhang, Y., Kerstetter, R.A., Michael, T.P., and, Lam, E., (2013) Integrative analysis of chromatin states in Arabidopsis identified potential regulatory mechanisms for natural antisense transcript production. Plant J. 73, 77-90.
24. Lynch, V.J., Leclerc, R.D., May, G., and, Wagner, G.P., (2011) Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat. Genet. 43, 1154-1158.
25. Medstrand, P., van de Lagemaat, L.N., Dunn, C.A., Landry, J.R., Svenback, D., and, Mager, D.L., (2005) Impact of transposable elements on the evolution of mammalian gene regulation. Cytogenet. Genome Res. 110, 342-352.
26. Miele, V., Penel, S., and, Duret, L., (2011) Ultra-fast sequence clustering from similarity networks with SiLiX. BMC Bioinformatics, 12, 116.
27. Naouar, N., Vandepoele, K., Lammens, T., et al. (2009) Quantitative RNA expression analysis with Affymetrix Tiling 1.0R arrays identifies new E2F target genes. Plant J. 57, 184-194.
28. Ouyang, S., Zhu, W., Hamilton, J., et al. (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res. 35, D883-D887.
29. Quinlan, A.R., and, Hall, I.M., (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26, 841-842.
30. Ramirez-Parra, E., Fründt, C., and, Gutierrez, C., (2003) A genome-wide identification of E2F-regulated genes in Arabidopsis. Plant J. 33, 801-811.
31. Ramirez-Parra, E., del Pozo, J.C., Desvoyes, B., de la Paz Sanchez, M., and, Gutierrez, C., (2007) E2F-DP transcription factors. In Annual Plant Reviews: Cell Cycle Control and Plant Development., Vol. 32 (D. Inze., ed.) Oxford: Blackwell Publishing Ltd, pp. 138-163.
32. Richard, G.F., Kerrest, A., and, Dujon, B., (2008) Comparative genomics and molecular dynamics of DNA repeats in eukaryotes. Microbiol. Mol. Biol. Rev. 72, 686-727.
33. Schmidt, D., Schwalie, P.C., Wilson, M.D., Ballester, B., Goncalves, A., Kutter, C., Brown, G.D., Marshall, A., Flicek, P., and, Odom, D.T., (2012) Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell, 148 (1-2), 335-348.
34. Slotkin, R.K., Vaughn, M., Borges, F., Tanurdzic̈, M., Becker, J.D., Feijó, J.A., and, Martienssen, R.A., (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell, 136, 461-472.
35. de Souza, F.S.J., Franchini, L.F., and, Rubinstein, M., (2013) Exaptation of transposable elements into novel cis-regulatory elements: is the evidence always strong? Mol. Biol. Evol. 30, 1239-1251.
36. Takeda, S., Sugimoto, K., Otsuki, H., and, Hirochika, H., (1999) A 13-bp cis-regulatory element in the LTR promoter of the tobacco retrotransposon Tto1 is involved in responsiveness to tissue culture, wounding, methyl jasmonate and fungal elicitors. Plant J. 18, 383-393.
37. Testori, A., Caizzi, L., Cutrupi, S., Friard, O., De Bortoli, M., Cora, D., and, Caselle, M., (2012) The role of transposable elements in shaping the combinatorial interaction of transcription factors. BMC Genomics, 13, 400.
38. Vandepoele, K., Vlieghe, K., Florquin, K., Hennig, L., Beemster, G.T., Gruissem, W., Van de Peer, Y., Inze, D., and, De Veylder, L., (2005) Genome-wide identification of potential plant E2F target genes. Plant Physiol. 139, 316-328.
39. Wang, T., Zeng, J., Lowe, C.B., Sellers, R.G., Salama, S.R., Yang, M., Burgess, S.M., Brachmann, R.K., and, Haussler, D., (2007) Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc. Natl Acad. Sci. USA, 104, 18613-18618.
40. Wang, J.R., Bowen, N.J., Marino-Ramirez, L., and, Jordan, I.K., (2009) A c-Myc regulatory subnetwork from human transposable element sequences. Mol. BioSyst. 5, 1831-1839.
41. Zhang, Y., Liu, T., Meyer, C.A., et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137.
42. Zheng, N., Fraenkel, E., Pabo, C.O., and, Pavletich, N.P., (1999) Structural basis of DNA recognition by the heterodimeric cell cycle transcription factor E2F-DP. Genes Dev. 13, 666-674.