The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana

Plant Journal

Volumn 68, Issue 4, 2011, Pages 646-656

  Heckmann, Stefan ^a   Lermontova, Inna ^a   Berckmans, Barbara ^b,c   De Veylder, Lieven ^b,c   Bäumlein, Helmut ^a   Schubert, Ingo ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

Arabidopsis thaliana; CENH3 promoter; centromere; E2F DP RBR transcription factors; IME intron; kinetochore

Indexed keywords

ARABIDOPSIS THALIANA; CENH3 PROMOTER; CENTROMERE; E2F/DP/RBR TRANSCRIPTION FACTORS; IME/INTRON; KINETOCHORE;

BINDING SITES; GENES; TISSUE; TRANSCRIPTION FACTORS;

TRANSCRIPTION;

ARABIDOPSIS PROTEIN; HISTONE; TRANSCRIPTION FACTOR E2F;

ARABIDOPSIS; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; PROMOTER REGION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; CHROMATIN IMMUNOPRECIPITATION; E2F TRANSCRIPTION FACTORS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, PLANT; HISTONES; PROMOTER REGIONS, GENETIC;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 80855130721     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04715.x     Document Type: Article

References (68)

1. Allshire, R.C., and, Karpen, G.H., (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat. Rev. Genet. 9, 923-937. (Pubitemid 50329068)
2. Amato, A., Schillaci, T., Lentini, L., and, Di Leonardo, A., (2009) CENPA overexpression promotes genome instability in pRb-depleted human cells. Mol. Cancer, 8, 119.
3. Ascencio-Ibanez, J.T., Sozzani, R., Lee, T.J., Chu, T.M., Wolfinger, R.D., Cella, R., and, Hanley-Bowdoin, L., (2008) Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol. 148, 436-454. (Pubitemid 352847618)
4. Berckmans, B., and, De Veylder, L., (2009) Transcriptional control of the cell cycle. Curr. Opin. Plant Biol. 12, 599-605.
5. Borghi, L., Gutzat, R., Futterer, J., Laizet, Y., Hennig, L., and, Gruissem, W., (2010) Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell, 22, 1792-1811.
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. (Pubitemid 39218784)
7. Chaubet-Gigot, N., Kapros, T., Flenet, M., Kahn, K., Gigot, C., and, Waterborg, J.H., (2001) Tissue-dependent enhancement of transgene expression by introns of replacement histone H3 genes of Arabidopsis. Plant Mol. Biol. 45, 17-30. (Pubitemid 32176751)
8. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
9. De Veylder, L., Beeckman, T., Beemster, G.T.S., et al. (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J. 21, 1360-1368. (Pubitemid 34246514)
10. Donnelly, P.M., Bonetta, D., Tsukaya, H., Dengler, R.E., and, Dengler, N.G., (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev. Biol. 215, 407-419.
11. Dubin, M., Fuchs, J., Graf, R., Schubert, I., and, Nellen, W., (2010) Dynamics of a novel centromeric histone variant CenH3 reveals the evolutionary ancestral timing of centromere biogenesis. Nucleic Acids Res. 38, 7526-7537.
12. Dunleavy, E.M., Roche, D., Tagami, H., Lacoste, N., Ray-Gallet, D., Nakamura, Y., Daigo, Y., Nakatani, Y., and, Almouzni-Pettinotti, G., (2009) HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell, 137, 485-497.
13. Earnshaw, W.C., and, Rothfield, N., (1985) Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma, 91, 313-321. (Pubitemid 15106904)
14. Egelkrout, E.M., Mariconti, L., Settlage, S.B., Cella, R., Robertson, D., and, Hanley-Bowdoin, L., (2002) Two E2F elements regulate the proliferating cell nuclear antigen promoter differently during leaf development. Plant Cell, 14, 3225-3236. (Pubitemid 36029143)
15. Fang, Y., and, Spector, D.L., (2005) Centromere positioning and dynamics in living Arabidopsis plants. Mol. Biol. Cell, 16, 5710-5718. (Pubitemid 41752220)
16. Furuyama, T., Dalal, Y., and, Henikoff, S., (2006) Chaperone-mediated assembly of centromeric chromatin in vitro. Proc. Natl Acad. Sci. USA, 103, 6172-6177.
17. Hayashi, T., Fujita, Y., Iwasaki, O., Adachi, Y., Takahashi, K., and, Yanagida, M., (2004) Mis16 and Mis18 are required for CENP-A loading and histone deacetylation at centromeres. Cell, 118, 715-729. (Pubitemid 39221731)
18. Heun, P., Erhardt, S., Blower, M.D., Weiss, S., Skora, A.D., and, Karpen, G.H., (2006) Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev. Cell, 10, 303-315.
19. 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.
20. Inze, D., (2005) Green light for the cell cycle. EMBO J. 24, 657-662. (Pubitemid 40396096)
21. Jansen, L.E., Black, B.E., Foltz, D.R., and, Cleveland, D.W., (2007) Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176, 795-805. (Pubitemid 46425540)
22. Jefferson, R.A., Kavanagh, T.A., and, Bevan, M.W., (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907.
23. Jeong, Y.-M., Mun, J.-H., Lee, I., Woo, J.C., Hong, C.B., and, Kim, S.-G., (2006) Distinct roles of the first introns on the expression of Arabidopsis profilin gene family members. Plant Physiol. 140, 196-209. (Pubitemid 43956315)
24. Jeong, Y.M., Mun, J.H., Kim, H., Lee, S.Y., and, Kim, S.G., (2007) An upstream region in the first intron of petunia actin-depolymerizing factor 1 affects tissue-specific expression in transgenic Arabidopsis (Arabidopsis thaliana). Plant J. 50, 230-239. (Pubitemid 46624132)
25. Karimi, M., Inze, D., and, Depicker, A., (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195. (Pubitemid 36725938)
26. Karimi, M., Depicker, A., and, Hilson, P., (2007) Recombinational cloning with plant gateway vectors. Plant Physiol. 145, 1144-1154. (Pubitemid 350276733)
27. Lageix, S., Catrice, O., Deragon, J.M., Gronenborn, B., Pelissier, T., and, Ramirez, B.C., (2007) The nanovirus-encoded Clink protein affects plant cell cycle regulation through interaction with the retinoblastoma-related protein. J. Virol. 81, 4177-4185. (Pubitemid 46586912)
28. Lai, A., Lee, J.M., Yang, W.M., DeCaprio, J.A., Kaelin, W.G. Jr, Seto, E., and, Branton, P.E., (1999a) RBP1 recruits both histone deacetylase-dependent and -independent repression activities to retinoblastoma family proteins. Mol. Cell. Biol. 19, 6632-6641. (Pubitemid 29441847)
29. Lai, A., Marcellus, R.C., Corbeil, H.B., and, Branton, P.E., (1999b) RBP1 induces growth arrest by repression of E2F-dependent transcription. Oncogene, 18, 2091-2100. (Pubitemid 29178577)
30. Lam, A.L., Boivin, C.D., Bonney, C.F., Rudd, M.K., and, Sullivan, B.A., (2006) Human centromeric chromatin is a dynamic chromosomal domain that can spread over noncentromeric DNA. Proc. Natl Acad. Sci. USA, 103, 4186-4191.
31. Lammens, T., Boudolf, V., Kheibarshekan, L., et al. (2008) Atypical E2F activity restrains APC/C-CCS52A2 function obligatory for endocycle onset. Proc. Natl Acad. Sci. USA, 105, 14721-14726.
32. 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.
33. 2 and requires the presence of the histone fold domain. Plant Cell, 18, 2443-2451. (Pubitemid 44749881)
34. Lermontova, I., Fuchs, J., Schubert, V., and, Schubert, I., (2007) Loading time of the centromeric histone H3 variant differs between plants and animals. Chromosoma, 116, 507-510. (Pubitemid 350120986)
35. Lermontova, I., Rutten, T., and, Schubert, I., (2011) Deposition, turnover and release of CENH3 at Arabidopsis centromeres. Chromosoma, doi: 10.1007/s00412-011-0338-5.
36. Luo, R.X., Postigo, A.A., and, Dean, D.C., (1998) Rb interacts with histone deacetylase to repress transcription. Cell, 92, 463-473. (Pubitemid 28101110)
37. Magyar, Z., (2008) Keeping the balance between proliferation and differentiation by the E2F transcriptional regulatory network is central to plant growth and development. In Plant Growth Signaling (, Bögre, L., and, Beemster, G., eds). Berlin/Heidelberg: Springer, pp. 89-105.
38. Magyar, Z., De Veylder, L., Atanassova, A., Bako, L., Inze, D., and, Bogre, L., (2005) The role of the Arabidopsis E2FB transcription factor in regulating auxin-dependent cell division. Plant Cell, 17, 2527-2541.
39. Mariconti, L., Pellegrini, B., Cantoni, R., Stevens, R., Bergounioux, C., Cella, R., and, Albani, D., (2002) The E2F family of transcription factors from Arabidopsis thaliana- novel and conserved components of the retinoblastoma/E2F pathway in plants. J. Biol. Chem. 277, 9911-9919. (Pubitemid 34968097)
40. Menges, M., Hennig, L., Gruissem, W., and, Murray, J.A., (2003) Genome-wide gene expression in an Arabidopsis cell suspension. Plant Mol. Biol. 53, 423-442. (Pubitemid 38345338)
41. Meshi, T., Taoka, K.I., and, Iwabuchi, M., (2000) Regulation of histone gene expression during the cell cycle. Plant Mol. Biol. 43, 643-657.
42. Moraes, I.C., Lermontova, I., and, Schubert, I., (2011) Recognition of A. thaliana centromeres by heterologous CENH3 requires high similarity to the endogenous protein. Plant Mol. Biol. 75, 253-261.
43. Moreno-Moreno, O., Torras-Llort, M., and, Azorin, F., (2006) Proteolysis restricts localization of CID, the centromere-specific histone H3 variant of Drosophila, to centromeres. Nucleic Acids Res. 34, 6247-6255. (Pubitemid 44942745)
44. 1/S-phase transition in 'tobacco. Plant Cell, 14, 1847-1857. (Pubitemid 35002938)
45. del Pozo, J.C., Boniotti, M.B., and, Gutierrez, C., (2002) Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCFAtSKP2 pathway in response to light. Plant Cell, 14, 3057-3071. (Pubitemid 36029132)
46. del Pozo, J.C., Diaz-Trivino, S., Cisneros, N., and, Gutierrez, C., (2006) The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell, 18, 2224-2235. (Pubitemid 44484722)
47. Qian, Y.W., Wang, Y.C., Hollingsworth, R.E. Jr, Jones, D., Ling, N., and, Lee, E.Y., (1993) A retinoblastoma-binding protein related to a negative regulator of Ras in yeast. Nature, 364, 648-652. (Pubitemid 23274725)
48. Ranjitkar, P., Press, M.O., Yi, X., Baker, R., MacCoss, M.J., and, Biggins, S., (2010) An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol. Cell, 40, 455-464.
49. Ransom, M., Dennehey, B.K., and, Tyler, J.K., (2010) Chaperoning histones during DNA replication and repair. Cell, 140, 183-195.
50. Ravi, M., and, Chan, S.W., (2010) Haploid plants produced by centromere-mediated genome elimination. Nature, 464, 615-618.
51. Ravi, M., Kwong, P.N., Menorca, R.M., Valencia, J.T., Ramahi, J.S., Stewart, J.L., Tran, R.K., Sundaresan, V., Comai, L., and, Chan, S.W., (2010) The rapidly evolving centromere-specific histone has stringent functional requirements in Arabidopsis thaliana. Genetics, 186, 461-471.
52. Rose, A.B., Elfersi, T., Parra, G., and, Korf, I., (2008) Promoter-proximal introns in Arabidopsis thaliana are enriched in dispersed signals that elevate gene expression. Plant Cell, 20, 543-551. (Pubitemid 352843991)
53. Sabelli, P.A., and, Larkins, B.A., (2009) Regulation and function of retinoblastoma-related plant genes. Plant Sci. 177, 540-548.
54. Schallau, A., Kakhovskaya, I., Tewes, A., Czihal, A., Tiedemann, J., Mohr, M., Grosse, I., Manteuffel, R., and, Baumlein, H., (2008) Phylogenetic footprints in fern spore- and seed-specific gene promoters. Plant J. 53, 414-424. (Pubitemid 351172018)
55. Schuh, M., Lehner, C.F., and, Heidmann, S., (2007) Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr. Biol. 17, 237-243. (Pubitemid 46186017)
56. Shelby, R.D., Vafa, O., and, Sullivan, K.F., (1997) Assembly of CENP-A into centromeric chromatin requires a cooperative array of nucleosomal DNA contact sites. J. Cell Biol. 136, 501-513. (Pubitemid 27083754)
57. Shuaib, M., Ouararhni, K., Dimitrov, S., and, Hamiche, A., (2010) HJURP binds CENP-A via a highly conserved N-terminal domain and mediates its deposition at centromeres. Proc. Natl Acad. Sci. USA, 107, 1349-1354.
58. Sozzani, R., Maggio, C., Varotto, S., Canova, S., Bergounioux, C., Albani, D., and, Cella, R., (2006) Interplay between Arabidopsis activating factors E2Fb and E2Fa in cell cycle progression and development. Plant Physiol. 140, 1355-1366. (Pubitemid 43956220)
59. Sullivan, L., Boivin, C., Mravinac, B., Song, I., and, Sullivan, B., (2011) Genomic size of CENP-A domain is proportional to total alpha satellite array size at human centromeres and expands in cancer cells. Chromosome Res. 19, 457-470.
60. Takahashi, K., Takayama, Y., Masuda, F., Kobayashi, Y., and, Saitoh, S., (2005) Two distinct pathways responsible for the loading of CENP-A to centromeres in the fission yeast cell cycle. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 595-606.
61. Taylor-Harding, B., Binne, U.K., Korenjak, M., Brehm, A., and, Dyson, N.J., (2004) p55, the Drosophila ortholog of RbAp46/RbAp48, is required for the repression of dE2F2/RBF-regulated genes. Mol. Cell. Biol. 24, 9124-9136. (Pubitemid 39313915)
62. Tomonaga, T., Matsushita, K., Yamaguchi, S., Oohashi, T., Shimada, H., Ochiai, T., Yoda, K., and, Nomura, F., (2003) Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. Cancer Res. 63, 3511-3516. (Pubitemid 36793029)
63. Van Hooser, A.A., Ouspenski, I.I., Gregson, H.C., Starr, D.A., Yen, T.J., Goldberg, M.L., Yokomori, K., Earnshaw, W.C., Sullivan, K.F., and, Brinkley, B.R., (2001) Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J. Cell Sci. 114, 3529-3542. (Pubitemid 33019769)
64. Vandepoele, K., Vlieghe, K., Florquin, K., Hennig, L., Beemster, G.T.S., 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. (Pubitemid 43951615)
65. Vandepoele, K., Quimbaya, M., Casneuf, T., De Veylder, L., and, Van de Peer, Y., (2009) Unraveling transcriptional control in Arabidopsis using cis-regulatory elements and coexpression networks. Plant Physiol. 150, 535-546.
66. Vermaak, D., Hayden, H.S., and, Henikoff, S., (2002) Centromere targeting element within the histone fold domain of Cid. Mol. Cell. Biol. 22, 7553-7561.
67. Waterborg, J., and, Robertson, A., (1996) Common features of analogous replacement histone H3 genes in animals and plants. J. Mol. Evol. 43, 194-206. (Pubitemid 26315121)
68. Wonsey, D.R., and, Follettie, M.T., (2005) Loss of the forkhead transcription factor FoxM1 causes centrosome amplification and mitotic catastrophe. Cancer Res. 65, 5181-5189. (Pubitemid 40827327)